The Control of Root Architecture by Lateral Root Formation

Review

April0???Tansley 2008 review review TansBlackwellOxford,NPHNew0028-646X1469-8137© The Phytologist Authors UK Publishing (2008). Ltd Journal compilation ley© New Phytologist (2008) reviewTansley review Branching out in new directions: the control of root architecture by lateral root formation

Author for correspondence: C. Nibau*, D. J. Gibbs* and J. C. Coates J. C. Coates School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK Tel: +44 121 414 5478 Fax: +44 121 414 5925 Email: [email protected] Received: 21 December 2007 Accepted: 14 March 2008

Contents

Summary 595 V. Transcriptomic studies to identify potential new regulators of lateral root development 608 I. Background 595 VI. Conclusions and future challenges 608 II. Formation of lateral roots 596 Acknowledgements 608 III. Endogenous factors regulating the stages of lateral root development 597 References 609

IV. Plasticity: modification of lateral root development by the environment 603

Summary

Key words: abiotic stress, biotic stress, Plant roots are required for the acquisition of water and nutrients, for responses to lateral root development, nutrients, plant abiotic and biotic signals in the soil, and to anchor the plant in the ground. Controlling hormones, root system architecture, plant root architecture is a fundamental part of plant development and evolution, transcriptomics. enabling a plant to respond to changing environmental conditions and allowing plants to survive in different ecological niches. Variations in the size, shape and surface area of plant root systems are brought about largely by variations in root branching. Much is known about how root branching is controlled both by intracellular signalling pat- hays and by environmental signals. Here, we will review this knowledge, with particular emphasis on recent advances in the field that open new and exciting areas of research. New Phytologist (2008) 179: 595–614 © The Authors (2008). Journal compilation © New Phytologist (2008) doi: 10.1111/j.1469-8137.2008.02472.x

structural anchor to support the shoot. The root system I. Background communicates with the shoot, and the shoot in turn sends A plant’s root system is the site of water and nutrient uptake signals to the roots. A plant root system initially consists of a from the soil, a sensor of abiotic and biotic stresses, and a primary root (PR) formed during embryogenesis that has dividing cells in a meristem at its tip. As the seedling develops, *These authors contributed equally to this work. certain other cells within the PR acquire the capability to

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hair development, primary root (PR) growth and AR formation. However, an extensive analysis of how these structures are controlled is outside the scope of the present review and the reader is referred to several other excellent reviews (Dolan & Costa, 2001; Carol & Dolan, 2002; Scheres et al., 2002; Casson & Lindsey, 2003; Hochholdinger et al., 2004; Samaj et al., 2004; Serna, 2005; Scheres, 2007). Moreover, colonization of certain plant roots by symbiotic bacteria or fungi leads to the formation of modified LRs (root nodules, mycorrhizas or proteoid roots) that carry out specialized functions such as nutrient acquisition (Oldroyd & Downie, 2004, 2006; Autran et al., 2006). In addition to signals that regulate many components of Fig. 1 Components of the root system. (a) A typical dicot RSA (and sometimes also shoot development), there is (e.g. Arabidopsis) seedling root system, consisting of a primary mounting evidence that some signalling networks are specific root (PR) originating from the embryo, lateral roots (LR) branching for LR formation (Rogg et al., 2001; Hochholdinger et al., out from the PR during seedling development, and root hairs 2004; Loudet et al., 2005; Coates et al., 2006), potentially (RH) that originate from PR epidermal (Epi) cells (shown at highlighting novel strategies for manipulating root branching higher magnification to the right (inset)). Ultimately, the LRs will undergo higher-order branching to form secondary and in crop plants. tertiary LRs. Adventitious roots (AR) form at the shoot–root junction. Because of the major contribution they play in the control (b) A typical cereal (e.g. rice, maize) seedling root system consisting of RSA, this review focuses on LRs: how they arise and develop. of a primary root (PR) originating from the embryo, seminal roots (SR) It will pay particular attention to recent molecular and ‘omic’ that originate postembryonically close to the top of the primary root, developments that highlight the huge variety of genes, and crown roots (CR) that originate from the stem. PR, SR and CR all form LR and undergo higher-order branching. proteins and mechanisms that interact together to coordinate a process so central to plant development and survival.

divide, eventually forming new roots, called lateral roots (LRs) II. Formation of lateral roots (Fig. 1a). These branch out from the PR, greatly increasing the total surface area and mechanical strength of the root In flowering plants and gymnosperms, LRs initiate from a system and allow the plant to explore the soil environment. specialized cell layer in the PR called the pericycle. The Ultimately, millions of higher-order root branches can form, pericycle is the outermost cell layer of the vascular cylinder resulting in hundreds of miles of root system in a small area and consists of two distinct cell types corresponding to the of soil (Dittmer, 1937). New roots, called adventitious roots underlying vasculature (Dubrovsky & Rost, 2005; Parizot (AR), can also be formed postembryonically at the shoot–root et al., 2008; Fig. 2a,b). In Arabidopsis and most other dicots, junction, optimizing the exploration of the upper soil layers LRs are formed only from pericycle cells overlying the (Fig. 1a). In cereals such as rice and maize, root structure developing xylem tissue (the xylem pole pericycle) (Fig 2b). In becomes more complex, with the formation of additional other species, particularly cereals such as maize, rice and wheat, shoot-borne and postembryonic roots, which in turn undergo LRs arise specifically from the phloem pole pericycle, with higher-order branching (Hochholdinger et al., 2004; Hoch- additional contributions from the endodermis (De Smet et al., holdinger & Zimmermann, 2008; Fig. 1b). 2006a; Hochholdinger & Zimmermann, 2008; Fig. 2b). The root system architecture (RSA) of plants varies hugely Insights into the evolution of multicellular, branched root between species and also shows extensive natural variation systems come from ‘ancient’ plants. In a vascular nonseed within species, reflecting the plethora of environments in plant, the fern Ceratopteris, LRs arise from the endodermis which plants can grow (Cannon, 1949; Loudet et al., 2005; and may be regulated differently from those in flowering Osmont et al., 2007). Root system architecture manipulation plants (Hou et al., 2004). The bryophyte moss Physcomitrella is instrumental in the domestication and breeding of crop patens revealed a very ancient mechanism controlling the plants, because using water and nutrients from the soil in the development of tissues with a rooting function (Menand et al., most efficient manner affects a plant’s ability to survive in 2007). Physcomitrella possesses putative homologues of known stressful or poor soils. Changes in RSA can therefore have Arabidopsis LR regulators, many of which have no assigned huge impacts on the final yield of a crop (reviewed in de function (e.g. Axtell et al., 2007; Rensing et al., 2008). Dorlodot et al., 2007). Of the factors that control total RSA, Lateral root formation consists of four key stages: (i) LR formation and growth is one of the most important. stimulation and dedifferentiation of pericycle founder cells; Many of the hormonal and environmental signals affecting (ii) cell cycle re-entry and asymmetric cell divisions to give rise LR development also affect other components that have a to a lateral root primordium (LRP); (iii) LRP emergence bearing on RSA and the overall root surface area, namely, root through the outer layers of the PR via cell expansion; and (iv)

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Fig. 2 Root anatomy. (a) Longitudinal section through an Arabidopsis primary root tip, showing the different cell types. LRC, lateral root cap (which is absent further up the root); Epi, epidermis (which is the outermost layer of the root above the root tip); Co, cortex; En, endodermis; P, pericycle; Vasc, vasculature (xylem and phloem); QC, quiescent centre (maintains the neighbouring stem cell population). (b) Transverse section through an Arabidopsis primary root. Epi, epidermis; RH, root hair; Co, cortex; En, endodermis; P, pericycle; XPP, xylem pole pericycle (the pericycle cells adjacent to the xylem tissue, from which lateral roots arise); Xy, xylem; Ph, phloem. In monocots, lateral roots arise from the phloem pole pericycle.

Fig. 3 Aspects of auxin signalling during lateral root (LR) development. (a) A pulse of auxin (light grey) in the basal meristem (BM) primes a pericycle cell (dark grey) to become competent to form a lateral root initial cell. (b) Cells (white) leaving the basal meristem between cyclical auxin maxima are not specified to become LR initials. (c) The first primed pericycle cell arrives at a point where it can initiate LR development; meanwhile another pericycle cell (dark grey) is primed in the basal meristem by the subsequent auxin pulse. (d) Lateral root initiation begins with auxin-induced IAA14 degradation. This allows activation of the ARF7 and ARF19 transcription factors, which activate expression of LBD/ ASL genes. LBD/ASL proteins in turn activate cell cycle genes and cell patterning genes, enabling formation of a new lateral root primordium (LRP). Auxin also activates transcription of NAC1 to stimulate LR initiation, and at the same time induces expression of two ubiquitin ligases, CEGUENDO and SINAT5, which feed back to attenuate the auxin response. activation of the LR meristem that recapitulates PR growth inducible system revealed that over 10% of the Arabidopsis (Celenza et al., 1995; Cheng et al., 1995; Laskowski et al., seedling root transcriptome was affected by treatment with 1995; Malamy & Benfey, 1997). auxin (Himanen et al., 2002; Vanneste et al., 2005). Auxin maxima appear at LR initiation sites and also later during emergence and elongation (see section III.1). Auxin III. Endogenous factors regulating the stages of ‘hot spots’ within the root arise as a result of the regulated lateral root development positioning of auxin transporters within cells, in a process Underpinning each stage of LR development is the hormone conserved between lateral organ formation in the root and in auxin (Casimiro et al., 2003; Woodward & Bartel, 2005; the shoot (Benkova et al., 2003). Interestingly, auxin signalling Figs 3a–d and 4a–d). Comprehensive studies using a LR- regulates the differential positioning of auxin efflux carriers

Fig. 4 Lateral root development in Arabidopsis shown in longitudinal section. P, pericycle; En, endodermis; Co, cortex; Epi, epidermis. (a) Early initiation – a founder xylem pole pericycle cell (dark grey) undergoes initial anticlinal cell divisions (perpendicular to the surface of the root). (b) Periclinal cell divisions (parallel to the surface of the root) begin and the lateral root primordium (LRP) begins to grow. (c) The LRP undergoes further organized cell divisions and begins to emerge through the outer cell layers of the primary root, resulting in cell separation (asterisks). (d) The new lateral root is fully emerged and its new meristem is activated (dark grey star). It will continue to grow and elongate. At each stage, the effect of various key plant hormones is indicated. ABA, abscisic acid; BR, brassinosteroids.

and, consequently, the direction of auxin flow (Sauer et al., differential cell cycle regulation between pericycle cell types. 2006). This effect is mediated by the activity of VPS29, a Normally, not all xylem pole pericycle cells form LRP, membrane-trafficking component that is involved in the indicating that multiple levels of control occur in these cells recycling of cargo molecules. Together with other proteins, (Beeckman et al., 2001). However, exogenous application of VPS29 mediates the dynamic arrangement of auxin efflux auxin can activate the whole pericycle to form LRPs, whereas carriers in response to auxin (Jaillais et al., 2007). The regulated the application of auxin transport inhibitors blocks LR interplay between auxin transport and signalling is critical for formation without loss of pericycle identity (Casimiro et al., all stages of LR development, and many of the signals regulating 2001; Himanen et al., 2002). Therefore, all the cells within RSA impinge upon this pathway. the pericycle retain the ability to form LRs but only some of Many Arabidopsis and cereal mutants affecting auxin pro- them do so. It is thus suggested that the coordinated action of duction, transport and metabolism have LR defects: their auxin transport and signalling, cell cycle regulators and novel involvement in LR formation has been described extensively root-specific proteins is necessary for LR initiation to occur. elsewhere (Casimiro et al., 2003; Woodward & Bartel, 2005; Fukaki et al., 2007). Lack of detailed characterization of many Lateral root initiation requires auxin and regulated protein of these mutants prevents identification of the particular stage degradation Auxin signalling during LR initiation is closely of LR development at which they act (De Smet et al., 2006a). coupled with regulated protein degradation (Fig. 3d). Proteins Exhaustive description of all the proteins involved in are targeted to the cellular degradation machinery, the auxin-dependent lateral organ formation is beyond the scope proteasome, by the addition of a chain of ubiquitin monomers. of this review and the reader is directed to recent reviews in The process requires a ubiquitin-activating enzyme (E1), a this area (De Smet et al., 2006a; Teale et al., 2006; De Smet ubiquitin-conjugating enzyme (E2) and a ubiquitin-protein & Jurgens, 2007). ligase (E3), which transfers ubiquitin from the E2 to the Other hormone pathways are also involved in the regulation target (Petroski & Deshaies, 2005). Some E3 ubiquitin ligases of LR formation, and recent research provides new insight consist of multiprotein complexes, and SKP1-CULLIN1-F-box into these pathways. Below we will outline how plant hor- (SCF) E3 ligases contain F-box protein subunits that confer mones, with particular emphasis on auxin, interact with various specificity, binding to particular target proteins. cellular processes to control each stage of LR development. Auxin receptors are a family of F-box-containing proteins known as TIR1 and AFB1–3 (Dharmasiri et al., 2005a,b; Kepinski & Leyser, 2005). It is thus not surprising that 1. Lateral root initiation – stimulation of cell cycle mutants in components of the SCF complex and its associated proliferation in the pericycle proteins have altered LR phenotypes (Gray et al., 1999; Hell- In Arabidopsis, the xylem pole pericycle cells, from which LRs mann et al., 2003; Bostick et al., 2004; Chuang et al., 2004; arise, are smaller than other pericycle cells, indicating Woodward et al., 2007).

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Auxin binding to TIR1/AFBs allows them to interact with 2007). It will be important to determine whether IAA14/ AUX/IAA proteins and target them for degradation. AUX/IAA SLR1 stability or cell cycle gene expression is affected in vfb proteins are transcriptional repressors that dimerize with mutants. auxin response factor (ARF) transcription factors, preventing The NAC1 transcription factor promotes LR initiation the latter from binding to promoter elements in auxin- (Xie et al., 2000) and may bind auxin-responsive promoters responsive genes. Thus, auxin-induced degradation of AUX/ to transmit the auxin signal (Fig. 3d). Interestingly, NAC1 IAAs enables ARFs to activate auxin-responsive transcription overexpression can rescue the reduced LR phenotype of tir1 (Gray et al., 2001; Dharmasiri et al., 2005a,b; Kepinski & auxin receptor mutants. NAC1 is tightly regulated: NAC1 Leyser, 2005). AUX/IAAs and ARFs exist as large, functionally expression is induced within 30 min of auxin application, redundant protein families (Okushima et al., 2005; Overvoorde suggesting that NAC1 may be an early auxin-responsive gene. et al., 2005). Auxin also induces the expression (albeit more slowly) of One of the most important AUX/IAA proteins for LR SINAT5, a RING-finger ubiquitin E3 ligase (Fig. 3d). SINAT5 initiation is SLR1/IAA14. As a result of the stabilization promotes NAC1 ubiquitination and subsequent degradation of IAA14, a gain-of-function slr1 mutant does not form LRs (Xie et al., 2002). It will be interesting to determine if auxin (Fukaki et al., 2002). In wild-type plants, auxin triggers binds directly to SINAT5 in the SINAT5–NAC1 complex. the degradation of IAA14, enabling ARF7 and ARF19 to Yet another ubiquitin ligase involved in LR initiation is activate transcription of LATERAL ORGAN BOUNDARIES XBAT32 (Nodzon et al., 2004). XBAT32 is a RING-finger DOMAIN/ASYMMETRIC LEAVES LIKE (LBD/ASL) genes protein highly expressed in the vascular system close to sites of (Fukaki et al., 2005; Okushima et al., 2007; and Fig. 3d). LR initiation. Plants lacking XBAT32 develop fewer LRs than LBD/ASL proteins, in turn, activate the transcription of cell wild-type plants and have reduced cell division in the pericycle. proliferation and patterning genes (Okushima et al., 2007). XBAT32 may be involved in auxin transport: loss of XBAT32 In maize and rice, LBD genes regulate shoot-borne root may lead to suboptimal auxin levels for LR initiation (Nodzon formation rather than LRs (Taramino et al., 2007; Hoch- et al., 2004). holdinger & Zimmermann, 2008). ARF7 also interacts with As only certain pericycle cells usually give rise to LRs, it is a MYB transcription factor that provides a link among auxin, crucial that auxin signals are tightly regulated. Interestingly, LR initiation and environmental responses (Shin et al., 2007; auxin stimulates the transcription of ubiquitin ligases that and section IV.4). repress auxin signals, providing an elegant feedback mechanism Comparison of the auxin-induced transcriptomes of to maintain auxin sensitivity in the pericycle. The F-box wild-type and slr1 roots identified 913 specific ‘LR initiation’ protein CEGENDUO (CEG) is a negative regulator of LR genes that function downstream of the auxin/slr1 signalling formation whose transcription is induced by auxin (Dong pathway. Many of these are cell cycle-associated genes or cell et al., 2006; and Fig. 3d). Further studies are needed to clarify division-associated genes, and genes involved in auxin signalling, its role LR initiation. transport or metabolism. Other over-represented functional It is thus clear that the action of auxin during LR initiation categories include macromolecular biosynthesis, ribosome depends heavily on the ubiquitin-proteasome pathway, both biogenesis and DNA synthesis (Vanneste et al., 2005). to transduce signals by degrading repressors and also to reset IAA28 is also important for LR initiation. The gain-of- the system by destroying activators when they are no longer function mutant iaa28 forms fewer LRs than the wild type: needed. Protein degradation allows for rapid changes in IAA28 is degraded by auxin and represses auxin-induced response to the ever-changing environment, as well as provid- LR-formation genes. However, IAA28 mRNA levels are ing fine-tuning to sustained signals. repressed by auxin, indicating a complex regulation of IAA28 during auxin signalling (Rogg et al., 2001; Dreher et al., Which pericycle cells? Questions remain about where, when 2006). The iaa28 mutant is also resistant to exogenous cyto- and which pericycle cells are primed to become LR initiation kinins and ethylene, suggesting an integration point for other sites. In the last year, this problem has been addressed by new hormone pathways. molecular genetic and mathematical modelling studies. The VIER F-BOX PROTEINE (VFB) F-box proteins De Smet et al. (2007) showed that the position of Arabidopsis are also important for LR formation in Arabidopsis. Mutants LR formation is determined in a region at the transition between deficient in VFB function have reduced LR formation. Micro- the meristem and the elongation zone, called the basal meristem array analysis demonstrated that loss of VFB function leads to (Fig. 3a–c). Lateral roots occurred in a regularly spaced alternating altered expression of both auxin-responsive genes and cell left–right pattern correlating with gravity-induced root waving. wall-remodelling genes (Schwager et al., 2007). Despite this, Both responses are dependent on the auxin influx transporter, vfb mutant plants maintain full sensitivity to exogenously AUX1. Furthermore, auxin responsiveness at the basal meristem applied auxin. VFBs may regulate auxin-induced gene exp- oscillates in a periodic manner, correlating with the timing of ression, and consequently LR formation, by a pathway LR formation. This, together with the observation of a lateral independent of the auxin receptor TIR1 (Schwager et al., gradient of auxin responsiveness with a maximum in protoxylem

cells, led the authors to suggest that auxin accumulation the proportion of active chromatin in the genome (De alone is sufficient for the priming of founder cells (De Smet Veylder et al., 2007). Indeed, a chromatin remodelling factor et al., 2007). Consequently, one can suggest that all the other mutant has perturbed LR initiation (Fukaki et al., 2006). Cell factors involved in LR formation will act downstream of the cycle progression from G1 to S requires the activity of the auxin signal. However, several factors have been suggested to retinoblastoma (RB)-E2F pathway (del Pozo et al., 2006; De regulate LR formation independently of auxin (see section Veylder et al., 2007). Progression from G2 to M is regulated III.1 ‘Hormone-independent signalling pathways that regulate by the opposing activity of B-type cyclin-dependent kinases lateral root initiation’). Targeted manipulation of these genes (CDKs) and CDK inhibitor proteins (KRPs) (Wang et al., in pericycle cells in the basal meristem is necessary to clarify 1997; De Veylder et al., 2001; Verkest et al., 2005). Many cell this conundrum. In addition, it is well known that environ- cycle components are transcriptionally regulated by auxin mental factors can tap into the LR developmental program (Himanen et al., 2002; Vanneste et al., 2005). Another level and alter root architecture in regions outside the basal meristem of regulation involves cell cycle protein degradation (Verkest (see section IV). et al., 2005; del Pozo et al., 2006). Support for the co-regulation of LR formation and gravi- In tomato, nitric oxide is required in the early stages of LR tropism came from a mathematical model suggesting that formation to regulate the expression of cell cycle genes, down- gravistimulation concentrates auxin at a certain point in the stream of the auxin signal (Correa-Aragunde et al., 2006). root, allowing the auxin threshold necessary for LR formation Nitric oxide is also induced in Arabidopsis LRP by the auxin, to be reached. Lateral root initiation would, in turn, consume indole-3-butyric acid (Kolbert et al., 2007). the auxin pool in that area, preventing new LR initiation until Despite the importance of the cell cycle in LR initiation, the pool had been refilled: this would be accelerated by a new increasing the mitotic index in roots or forcing excessive cell gravistimulation (Lucas et al., 2007). Two main ideas came divisions in the pericycle does not stimulate LR initiation or out of this study: first, there is an endogenous mechanism morphogenesis (Vanneste et al., 2005; Wang et al., 2006). regulating the periodicity of LR formation, revealed by the Thus, pericycle cell divisions can be uncoupled from LRP existence of a minimum and maximum time between two formation, and LR initiation seems to require the simultaneous successive LR initiations. Second, this endogenous system is activation of cell cycle and cell fate genes triggered by auxin- sensitive to external cues such as gravity (Lucas et al., 2007). induced degradation of the SLR/IAA14 protein (Vanneste This would provide increased plasticity for the root system to et al., 2005). Conversely, although cell division and LR adapt to new soil conditions. morphogenesis are both controlled by auxin signalling, the Interestingly, the developmental window for LR initiation processes are regulated independently, as shown by tomato in Arabidopsis displays natural variation between accessions diageotropica (dgt) mutants that have a number of auxin-related (Dubrovsky et al., 2006), which may indicate adaptation of phenotypes (including a lack of LRs) but have normal root the system to different environmental niches. In addition, cell identities and patterning. dgt mutant pericycle cells maintain LRP initiation and emergence are separable processes, again their full proliferative capacity, but no LRs are formed, even providing greater plasticity to the root system (Dubrovsky in the presence of exogenous auxin, which instead stimulates et al., 2006). The mathematical model used by Lucas et al. further pericycle divisions to form multiple cell layers (2007) suggests that LR formation in gravistimulated areas (Ivanchenko et al., 2006). A similar mechanism operates in may also optimize soil exploration. It will be interesting to Arabidopsis, as demonstrated by the wol mutant, which forms determine if biotic and abiotic factors that alter RSA also have very few LRs even in the presence of auxin (Parizot et al., an effect on gravitropism-stimulated LR formation. 2008). Close analysis of the pericycle cells in the wol mutant It is important to move this type of research beyond showed that they express pericycle protoxylem markers and Arabidopsis to agriculturally relevant plants, especially as the are able to divide in response to auxin but no LRPs are formed mechanisms at work in crop plants may differ from those (Parizot et al., 2008). This again shows that cell cycle activation in Arabidopsis. In many grasses, LRs initiate in phloem pole is not sufficient for LR initiation to occur. pericycle cells and, because of varying root organization and Heterotrimeric G-proteins may integrate auxin signalling and growth rates, the timing and spacing of LR initiation is also cell cycle inputs during root branching as well as other develop- different (Dubrovsky et al., 2006; Dembinsky et al., 2007). mental processes (Ullah et al., 2001, 2003; Chen et al., 2006b; Tr u s ov et al., 2007). Mutations in the β or γ G-protein Interplay between the cell cycle and auxin signalling It is subunits show increased cell division and increased LR forma- generally accepted that pericycle cells are arrested in the G1 tion, and the normal function of Gβ and Gγ may be to attenuate phase of the cell cycle. Those pericycle cells that will give rise auxin signalling (Ullah et al., 2003; Trusov et al., 2007). to a LR proceed through S phase and arrest in G2. Lateral root-inducing signals stimulate these cells to undergo Other hormones affecting LR development In addition to proliferative cell divisions (Beeckman et al., 2001). Cell cycle auxin, other hormone signals are important for LR initia- re-entry requires changes in chromatin structure, increasing tion (Fig. 4a–d). Traditionally, cytokinin is thought to act

New Phytologist (2008) 179: 595–614 www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley revie w Review 601 antagonistically to auxin in many developmental processes: Curiously, ABA seems to stimulate LR initiation in rice (Chen indeed, cytokinin is a negative regulator of LR formation in et al., 2006a). many plant species, including Arabidopsis, Medicago, tobacco In addition to ‘classical’ plant hormones, several other signals and rice (Werner et al., 2003; Rani Debi et al., 2005; affect LR development both during initiation and at later Gonzalez-Rizzo et al., 2006; Li et al., 2006b; Laplaze et al., stages, in a variety of plant species. Salicylic acid promotes LR 2007). Plants with decreased cytokinin content have increased initiation, emergence and growth, possibly via crosstalk LR numbers (Werner et al., 2001, 2003; To et al., 2004; with cytokinin or auxin (Echevarria-Machado et al., 2007). Mason et al., 2005; Gonzalez-Rizzo et al., 2006; Riefler et al., Melatonin promotes lateral and AR formation while decreas- 2006), whereas exogenous cytokinin inhibits LR initiation by ing root length, similarly to the effects of auxin (Arnao & preventing pericycle cell cycle re-entry (Li et al., 2006b). An Hernandez-Ruiz, 2007). Alkamides are lipid-based secondary elegant study by Laplaze et al. (2007) showed that exogenous metabolites that are novel regulators of plant growth and cytokinin disrupts both LR initiation and the organization of development (Lopez-Bucio et al., 2006). They induce LR cell divisions within developing LRPs: these defects cannot be initiation and growth in Arabidopsis (Ramirez-Chavez et al., rescued by auxin. Targeted expression of cytokinin biosynthetic 2004), and regulate meristematic activity throughout the plant. and catabolic enzymes in specific cell types demonstrated that It is suggested that they regulate root pericycle cell activation, cytokinin activity is required very early in the LR formation possibly via cytokinin signalling (Lopez-Bucio et al., 2007). process (Laplaze et al., 2007). Importantly, disrupting cytokinin signalling in xylem pole pericycle cells leads to perturbation Hormone-independent signalling pathways that regulate of the auxin maximum in developing LRPs as a result of the lateral root initiation The best-characterized protein that reduced expression of PIN auxin transporter genes and regulates LR initiation, independently of hormone signalling, mislocalization of PIN proteins (Laplaze et al., 2007). is ABERRANT LATERAL ROOT FORMATION 4 (ALF4). Both ethylene and brassinosteroids affect LR formation via The Arabidopsis alf4 mutant shows a complete absence of LRs, an auxin-dependent pathway (Bao et al., 2004; Stepanova even in the presence of auxin (Celenza et al., 1995). Cells et al., 2005). In rice, a casein kinase 1 gene, OsCKI, is upregu- appear to be blocked at a premitotic stage of the cell cycle, lated by both brassinosteroid and abscisic acid (ABA) and but the identity of the xylem pole pericycle itself is not promotes lateral and AR formation as well as cell elongation. compromised. ALF4 is a nuclear-localized protein of unknown OsCKI may affect LR development by regulating endogenous function; a shorter protein generated by alternative splicing auxin levels (Liu et al., 2003). Transcriptomic analysis of localizes to the cytoplasm. Importantly, auxin has no effect on OsCKI-deficient plants revealed alteration of several signalling, ALF4 levels or intracellular localization (DiDonato et al., developmental, transcriptional and metabolic genes (Liu 2004). In the current model, ALF4 maintains the pericycle in et al., 2003). a ‘competent’ state for cell division, allowing input from other Unequivocal evidence for a role of ABA in LR initiation is LR-inducing signals, including auxin (DiDonato et al., 2004). not available. However, the ABA-insensitive mutant abi3 The alf4 mutant maintains full responsiveness to auxin shows decreased sensitivity to auxin-induced LR initiation inhibition of PR elongation, suggesting that LR formation is (Brady et al., 2003). Furthermore, 9-cis-epoxycarotenoid not a simple recapitulation of the developmental program dioxygenase genes (involved in ABA biosynthesis) are expressed producing PRs. in pericycle cells surrounding LR initiation sites (Tan et al., Other regulators of LR initiation, acting independently of 2003). It is tempting to suggest that ABA may restrain cell known pathways, are ARABIDILLO-1 and ARABIDILLO-2, proliferation outside the LR initiation site, although ABA which act redundantly to promote LR initiation in Arabidopsis being produced as a result of the stress caused by LR emergence (Coates et al., 2006). ARABIDILLOs are F-box proteins, cannot be excluded (De Smet et al., 2006b). Indeed, ABA suggesting that they form ubiquitin E3 ligases. Importantly, upregulates the expression of KRP1, a cell cycle inhibitor arabidillo mutants and ARABIDILLO-overexpressing plants (Wang et al., 1998). Some auxin-induced LR-initiation genes are able to respond to exogenous auxin similarly to wild-type had previously been described as ABA-repressed (Vanneste plants. In addition, auxin distribution in the root tip appears et al., 2005). Among these, AUXIN-INDUCED IN ROOT to be normal in arabidillo mutants, and auxin does not affect CULTURES 12 (AIR12) and IAA19 function in LR formation the nuclear localization of ARABIDILLO proteins (Coates (Neuteboom et al., 1999; Tatematsu et al., 2004). Thus, ABA et al., 2006; C. Nibau, J. Coates, unpublished). and auxin could have an antagonistic effect on LR initiation Transcriptomic comparison of wild-type, arabidillo mutant (Fig. 4a). Interestingly, the KNAT1 homeobox transcription and ARABIDILLO-overexpressing roots reveals changes in factor is expressed at the base of LR primordia (Truernit et al., some genes defined as pericycle-enriched and LR-enriched 2006) and is auxin-induced and ABA-repressed in LR pri- (Birnbaum et al., 2003; Levesque et al., 2006; https:// mordia (Soucek et al., 2007), suggesting a possible point of www.genevestigator.ethz.ch/), but no strong overlaps with integration for the two signals. Further research is needed to other recent LR data sets defined by auxin induction, VFB establish ABA as an inhibitor of LR initiation in Arabidopsis. signalling, LR emergence or red light signalling (Vanneste

et al., 2005; Laskowski et al., 2006; Molas et al., 2006; ration for its controlled breakdown as LRs emerge (Laskowski Schwager et al., 2007; J. Coates, unpublished). ARABIDIL- et al., 2006). How this differential pectin methylation is fully LOs might act very early in determining pericycle cell fate. controlled remains an intriguing question. Given the recent suggestion that this determination occurs at Various Arabidopsis studies have shown that cell wall- the basal meristem (section III.1 ‘Which pericycle cells?’) it remodelling enzymes are induced by auxin in roots (Neuteboom will be interesting to establish whether arabidillo mutants are et al., 1999; Himanen et al., 2004; Vanneste et al., 2005; affected in this process. Laskowski et al., 2006). Cell wall remodelling genes induced by auxin include a PME, PLAs, and also an expansin and a beta-xylosidase (Laskowski et al., 2006). AtPLA1 and AtPLA2 2. Redifferentiation to form a new meristem that are both upregulated steadily for up to 24 h after only a 15-min recapitulates the root organization pulse of auxin: this response is blocked in the slr1/iaa14 Lateral root primordium formation and emergence A series mutant. In addition, expression of both AtPLAs is much of well-characterized cell divisions gives rise to the LRP higher in LR initials than in the pericycle cells from which (Malamy & Benfey, 1997). The coordinated pattern of cell they arise (Laskowski et al., 2006). division is dependent on auxin signalling and on the activity The polygalacturonase (PG) family of cell wall-degrading of the PUCHI gene. PUCHI is expressed in pericycle cells that enzymes may help to ‘prime’ the PR cells to separate ready for will form the LRP and in the LRP itself. PUCHI encodes an LR emergence (Gonzalez-Carranza et al., 2007). An Arabidopsis APETALA2 (AP2) transcription factor that is upregulated by PG (PGAZAT) is expressed specifically in the cortical and auxin and acts downstream of auxin to restrict the area of cell epidermal cells overlying the future site of LR emergence. A proliferation within the LRP. PUCHI is also necessary for pgazat insertion mutant has no obvious LR phenotype, but it correct cell divisions within the LRP (Hirota et al., 2007). In is likely that functional redundancy exists. Interestingly, root rice, the EL5 RING finger ubiquitin E3 ligase maintains PGAZAT expression is auxin-inducible (Gonzalez-Carranza cell viability in the developing primordium. EL5 may act et al., 2007). downstream of auxin, cytokinin and JA to prevent meristematic cell death (Koiwai et al., 2007). The identity of the target Activation of the lateral root meristem and lateral root proteins and the involvement of EL5 in LRP hormone elongation Activation and maintenance of the LR meristem signalling pathways remain to be investigated. requires polarized auxin transport to create an auxin maximum Once an LRP has initiated, it must form a functional at the tip of the LRP: this requires regulated activity of auxin meristem and emerge from within the parent root tissues. As influx and efflux transporters. During LR development there a result of rounds of cell division, the LRP increases in size, is an important change in the direction of auxin flow, brought forming a dome-shaped structure that penetrates the external about by AUX/IAA-dependent repositioning of auxin efflux cell layers of the PR. This requires separation of cells in the carriers towards the tip of the newly formed LR. This results endodermis, cortex and epidermis for the passage of the LR to in LR growth perpendicular to the PR (Benkova et al., 2003; the outside (Fig. 4c,d). This process must be tightly regulated, Sauer et al., 2006). The new LRP auxin maximum regulates as cell separation (particularly of the protective epidermal the activity of several transcription factors (Blilou et al., 2005). layer) constitutes a risk to the plant, potentially allowing the It is proposed that regulated expression of known regulators entry of pathogens from the soil into internal tissues. of PR meristem formation, such as the PLETHORA, Much less is known about how LRs emerge than how they CLAVATA, SCARECROW and SHORT ROOT, is also initiate. Changes in electrical potential occur around prospective important for the maintenance of an active meristem in LRs sites of LR emergence (Hamada et al., 1992) and auxin seems downstream of auxin (for a recent review see Scheres, 2007). to be required for LR emergence independently of its role Because mutations in these genes severely impair PR growth, in LR initiation. Shoot-derived auxin is required for LR emer- their effect on LR development has not been investigated: gence in Arabidopsis until c. 10 d after germination (Bhalerao targeted overexpression and underexpression in LRs will et al., 2002), and auxin can induce root cell separation in clarify this issue. Arabidopsis (Boerjan et al., 1995; Laskowski et al., 1995). Abscisic acid can reversibly block meristem activation Cell separation occurs via regulated activity of cell wall- postemergence by inhibiting the cell cycle gene expression remodelling enzymes. Breakdown of pectin is particularly necessary for meristem activity, leading to LR growth arrest important for cell separation, as the middle lamella between (De Smet et al., 2003). This effect of ABA defines a new adjacent cells is pectin-rich. Pectin is demethylated by pectin auxin-independent checkpoint between LR emergence and methylesterases (PMEs) before its catabolism. Pectin breakdown meristem activation, which may also be regulated by nitrate involves homogalacturonases called pectate lyases (PLAs). levels (De Smet et al., 2003). In line with this observation, an Interestingly, during LR emergence, the pectin in the emerging ABA receptor mutant is completely insensitive to ABA inhi- LR remains methylated, whereas the pectin in the overlying bition of LR development (Razem et al., 2006). No other parent root tissues becomes demethylated, possibly in prepa- known ABA-insensitive mutants show insensitivity, suggesting

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mutations in the auxin efflux transporter MDR1 cause nascent LRs to arrest their growth (Wu et al., 2007). The ALF3 protein elevates the levels of auxin at the LRP, probably by facilitating auxin transport (Celenza et al., 1995). The auxin-induced homeobox gene HAT2 may also modulate auxin distribution within the primordium (Sawa et al., 2002). Despite the fact that cytokinins inhibit LR initiation, they have a positive effect on LR elongation in Arabidopsis and rice, possibly via stimulation of cell cycle gene expression in an auxin-independent process (Rani Debi et al., 2005; Li et al., 2006b). Fig. 5 Lateral root responses to nutrient deprivation. When nitrate (N) levels are high, lateral root (LR) emergence and elongation is represssed compared with normal conditions. Locally high levels of N IV. Plasticity: modification of lateral root promote local LR proliferation. In low phosphate (P), primary root development by the environment growth ceases and LR density increases. In low sulphate (S), primary root growth and lateral root density increase, with LRs originating Plants are sessile organisms that need to survive in a dynamic closer to the root tip. In low potassium (K), LR elongation is inhibited. environment. Consequently, their root systems need to maintain plasticity to react to fluctuating abiotic and biotic factors. Genetically identical plants can have very different that ABA signalling during LR emergence involves specific RSA when grown in varying environmental conditions. Plants proteins (De Smet et al., 2003). ABI8, a plant-specific protein primarily respond to the abundance of macronutrients and of unknown function, is a possible novel signalling candidate. water to produce the best root network for optimum growth abi8 mutant plants are less sensitive to ABA and, despite and survival (Fig. 5). However, other exogenous factors, such being able to initiate LR, their LR meristem soon loses as plant–pathogen interactions, are also important for root competence to divide (Cheng et al., 2000; Brocard-Gifford development. An overview of the current understanding et al., 2004). of how changing external conditions affect RSA is presented This checkpoint between LR emergence and meristem here, with a particular focus on more recent advances. activation provides an elegant way by which environmental, nutritional and endogenous factors can modulate root archi- 1. Nitrogen availability and root system architecture: tecture through ABA signalling (Signora et al., 2001; De Smet local and global effects et al., 2006b; and section IV). For example, stress-induced oxylipin production affects LR development. Treatment of Inorganic nitrogen Root adaptation to nitrogen levels is an Arabidopsis seedlings with 9-hydroxyoctadecatrienoic acid excellent example of a plants’ developmental plasticity. Nitrogen (9-HOT), an oxylipin derivative, induces the accumulation of is available in the soil as ammonia, nitrite, nitrate and organic arrested early stage LRPs, accompanied by the upregulation nitrogen. The abundance of these compounds is highly of cell wall-associated genes (Vellosillo et al., 2007). The variable and can have dramatic effects on LR development. not-responding to oxylipins2 (noxy2) mutant has more LRs Species-specific differences in nitrogen responses are apparent: than the wild-type plant. 9-Hydroxyoctadecatrienoic acid and LR length, number or both can be affected (Zhang & Forde, related oxylipins are probably endogenous modulators of 1998; Linkohr et al., 2002; Boukcim et al., 2006). LR emergence that may act via ABA signalling and they are Nitrate levels have strongly opposing effects on LR growth, involved in RSA reprogramming in response to pathogen depending upon the context in which they occur. In low-nitrate infection (Vellosillo et al., 2007). soils, patches of high nitrate have a localized stimulatory effect Interestingly, ABA appears to have the opposite effect on on LR development in many species (Drew & Saker, 1975; LR emergence in legumes, stimulating LR formation in Zhang & Forde, 1998). However, where nitrate levels are Medicago (Liang & Harris, 2005). The Medicago latd mutant globally high (i.e. not growth limiting), LR growth is inhibited has a reduced root surface area with short PRs, arrested LRPs (Zhang et al., 1999). Thus, there are two clear morphological and disorganized meristems (Bright et al., 2005). The latd adaptations: a local stimulatory effect of exogenous nitrate phenotype can be at least partly rescued by the exogenous supply on LR elongation, and a systemic inhibitory effect of application of ABA, and latd mutants seem to be impaired in high nitrate on LR meristem activation. This is caused by the ABA perception or signalling (Liang et al., 2007). signalling effect of nitrate itself, rather than being a response Lateral root elongation occurs by cell division and elongation to downstream metabolites (Zhang & Forde, 1998). Some from the meristem and is controlled by several factors. Auxin species, including barley and cedar, but not Arabidopsis, are transport and signalling are important in this process. Auxin also able to respond to a localized ammonium supply (Drew, transport within the root is necessary for LR elongation, as 1975; Zhang et al., 1999; Boukcim et al., 2006).

Key protein players specific to the ‘local nitrate’ response Organic nitrogen Plants can use both organic nitrogen and include the Arabidopsis NITRATE REGULATED-1 (ANR1) inorganic nitrogen as a nutrient source. Arabidopsis roots show MADS-box transcription factor and the DUAL AFFINITY a specific set of responses to the amino acid l-glutamate, NITRATE TRANSPORTER (AtNRT1.1). Downregulation which inhibits PR growth and causes concomitant increases in of ANR1 reduces LR stimulation in nitrogen-rich zones, LR density to varying degrees in different ecotypes (Walch-Liu without compromising the overall nitrate-induced inhibition et al., 2006). This response is similar to roots grown in low of LRs (Zhang & Forde, 1998). Seven other MADS box genes phosphate, forming a short and highly branched RSA (section have a similar expression pattern to ANR1 under different IV.2; Williamson et al., 2001; Walch-Liu et al., 2006). nitrate conditions (Gan et al., 2005). Three of these (AGL-16, Root responses to l-glutamate are accompanied by dramatic AGL-21 and SOC1) interact with ANR1, although whether cytological changes, including microtubule depolymerization they represent nitrate signal transduction components is (Sivaguru et al., 2003). unknown (de Folter et al., 2005). The PR tip is the sensor for l-glutamate (as with phosphate; AtNRT1.1 is induced by nitrate (Munos et al., 2004) and section IV.2), which inhibits cell division in the meristem Atnrt1.1 mutants exhibit a strongly decreased response to (Walch-Liu et al., 2006). Interestingly, the auxin transport local nitrate supply (Liu et al., 1999). Interestingly, this mutant aux1 is somewhat insensitive to l-glutamate, whereas reduced responsiveness is accompanied by a reduction of the axr1 mutant (a modifier of auxin signalling and possibly ANR1 mRNA (Remans et al., 2006). Transporters have been also other hormone pathways) is hypersensitive to l-glutamate, previously identified as nutrient sensors, but it is unclear and various other auxin-signalling mutants exhibit wild- whether AtNRT1.1 is involved directly in nitrate sensing, or type sensitivity to l-glutamate (Walch-Liu et al., 2006). l- in facilitating access of nitrate to another sensor. glutamate probably acts as a signalling molecule rather than High nitrogen inhibits LR development after emergence as a nutritional cue, because closely related amino acids do not but before meristem activation. This effect is reversible: trans- elicit changes in root architecture (Walch-Liu et al., 2006). ferring plants to nitrate-limiting media results in a release of The molecular mechanism of l-glutamate perception at the LR inhibition within 24 h, so plants can respond rapidly to Arabidopsis root tip remains to be discovered. Interestingly, fluctuating environmental nitrate levels (Zhang & Forde, rice with a mutant putative glutamate receptor (OsGLR3.1) 1998). A high shoot nitrate status is important for the inhib- has short PRs and LRs, reduced cell division, and premature itory response, and an Arabidopsis mutant lacking nitrate differentiation and cell death in the root meristem (Li et al., reductase activity is hypersensitive to inhibition, suggesting 2006a). that systemic accumulation of nitrate causes LR inhibition Carnitine, an organic nitrogenous cation, induces LR (Zhang et al., 1999). formation. However, disruption of an Arabidopsis plasma How are nitrate responses regulated during LR development? membrane-localized carnitine transporter, AtOCT1, led Various ABA-deficient Arabidopsis mutants have significantly to increased root branching (Lelandais-Briere et al., 2007). reduced levels of LR inhibition in abundant nitrate (Signora AtOCT1 promoter activity is present in the root vasculature, et al., 2001). With both ABA and high nitrate, LRs are inhibited including at sites of LR initiation. This suggests a possible immediately after meristem activation (Signora et al., 2001; modulatory role for carnitine movement or homeostasis in the De Smet et al., 2003; and section III.1 ‘Other hormones control of RSA. It seems that AtOCT1 negatively regulates LR affecting LR development’). Arabidopsis LR ABA-insensitive development, and the local concentration of carnitine in the (LABI) mutants can still produce LRs in the presence of ABA: root may affect the C : N ratio and hence LR development they are also less sensitive to high nitrate, implying that the (Lelandais-Briere et al., 2007). inhibition of LRs by ABA and nitrate involves the same mechanism (Zhang et al., 2007a). Interestingly, transferring 2. Phosphorous: modulating total RSA but sensed at Arabidopsis and soybean from conditions of high nitrate to the root tip low nitrate increases root auxin (IAA) levels, suggesting that nitrate affects auxin synthesis or transport (Caba et al., 2000; Phosphorous is an essential nutrient, primarily taken up via Walch-Liu et al., 2000). the roots as inorganic phosphate (Pi). Phosphate is one of the Carbon : nitrogen (C : N) ratios affect RSA, further high- most inaccessible macronutrients in the soil, as it forms lighting the complexity of the root response to nitrate. A high insoluble compounds with metals in acidic and alkaline soils sucrose : nitrate ratio suppresses LRs, and a mutation in the (Raghothama, 1999). Root system architecture modifications high-affinity nitrate transporter AtNRT2.1 abolishes this in response to phosphate are critical for the fitness of the plant inhibition (Malamy & Ryan, 2001; Little et al., 2005). Like and differ from those seen with nitrate, perhaps reflecting a AtNRT1.1, AtNRT2.1 may be a direct nitrate sensor (Little Pi-foraging strategy, in contrast to nitrate responses that et al., 2005). In addition, AtNRT2.1 may have different improve nitrogen uptake (Fitter et al., 2002). functions depending on the degree and context of nitrate The main adaptive trait for accessing phosphate is the ability deficiency (Remans et al., 2006). to explore different layers near the soil surface through

New Phytologist (2008) 179: 595–614 www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley revie w Review 605 changes in the RSA (Lopez-Bucio et al., 2000). Various et al., 2005). In addition, Pi starvation affects gibberellin adaptations have evolved in different plants. In Arabidopsis, Pi signalling in roots, whereas gibberellin can attenuate the deficiency favours a redistribution of growth from the PR to low-Pi response (Jiang et al., 2007). LRs. The PR stops growing and the density and elongation of A variety of protein regulators of the phosphate-deficiency LRs increases, forming a shallow, highly branched root system response have been uncovered, which affect transcription, (Williamson et al., 2001; Lopez-Bucio et al., 2002). This translation and post-translational modifications. PHOS- prevents further growth into less nutrient-rich deeper soils, PHATE STARVATION RESPONSE-1 (PHR1) is an Arabi- increasing the exploration of the more nutrient-rich upper dopsis MYB-like transcription factor that regulates a number strata. In the bean Phaseolus vulgaris, a different strategy has of Pi-deficient responsive genes and is conserved in various evolved for achieving a similar explorative result: the angle of plant species (Rubio et al., 2001). Miura et al. (2005) reported root growth is shifted to predominantly outwards instead of that PHR1 is a target of the small ubiquitin modifier (SUMO) downwards when Pi levels are low (Bonser et al., 1996). The E3-ligase AtSIZ1 in vitro. Interestingly, Atsiz1 mutants exhibit nitrogen-fixing white lupin forms proteoid (cluster) roots that an exaggerated response to low Pi levels compared with wild secrete organic acids and phosphatases into the surrounding type, most notably an extensive increase in LR development soil to solubilize phosphate and aid its uptake (Schulze et al., and a stronger PR inhibition (Miura et al., 2005). Although 2006). no direct link between PHR1 and RSA modification has been Unlike nitrate responses, the initial effect of low-Pi sensing shown, two genes that belong to the PHR1 regulon (AtIPS1 is the arrest of PR growth, with changes in LRs occurring later. and AtRNS1) are positively regulated by AtSIZ1 during the Loss of PR growth occurs via reduced cell elongation and a initial stages of Pi limitation (Miura et al., 2005). However, it progressive loss of meristematic activity (Williamson et al., is unknown whether the root phenotype of Atsiz1 mutants is 2001; Sanchez-Calderon et al., 2005). The phosphate deficiency a result of PHR1 modification and subsequent downstream response-2 (pdr2) mutant displays hypersensitive inhibition of gene expression, or whether the effect is pleiotropic, as AtSIZ1 cell division in developing root meristems under Pi-limiting also has roles in other developmental pathways (Jin et al., conditions, suggesting that PDR2 is required for meristem 2008). function where external Pi is low. It therefore represents a Other transcription factors identified, but not fully charac- Pi-sensitive checkpoint that monitors Pi status and allows the terized as Pi-response components, include the basic leucine root system to adjust accordingly (Ticconi et al., 2004). In zipper (bZIP) transcription factor, PHI-2, in tobacco, and addition to soil Pi status, systemic Pi levels may also be more recently OsPTF1, a bHLH transcription factor providing important for the induction of Pi-deficient RSA responses tolerance to low-Pi conditions in rice (Sano & Nagata, 2002; (Williamson et al., 2001). Active photosynthesis, or the Yi et al., 2005). The WRKY75 transcription factor is strongly presence of sugar, is also essential for RSA responses to limiting induced during Pi deprivation (Devaiah et al., 2007). Several phosphate (Karthikeyan et al., 2007). genes are downregulated in plants with reduced levels of Physical contact of the Arabidopsis PR tip with low-Pi WRKY75, including high-affinity Pi transporters, which medium is necessary and sufficient to arrest primary growth consequently leads to reduced phosphate uptake during Pi and reprogram root architecture (Svistoonoff et al., 2007). starvation (Devaiah et al., 2007). WRKY75 may be a specific Multicopper oxidase mutants LOW PHOSPHATE ROOT-1 modulator of LR development (rather than affecting the PR) and -2 (LPR-1/-2) form long PRs in low Pi and provide and may also act independently of the Pi status of the plant to evidence that the root cap has an important role in nutrient modify LR development (Devaiah et al., 2007). sensing. Interestingly, LPR1 was previously identified as a quantitative trait locus (QTL) important for phosphate 3. Root responses to sulphur responses (Reymond et al., 2006). Despite highlighting a novel role for multicopper oxidases in plant development, it is Sulphur, in the form of sulphate, is required for the synthesis unknown whether LPRs are directly involved in the stimulation of methionine and cysteine and is critical for cellular of LR growth in low Pi. metabolism, growth and development, and stress responses. A variety of hormones may modify the Pi response. Sulphate deficiency is detrimental to a plant’s survival and Responses to low Pi correlate with increased auxin sensitivity leads to the development of a prolific root system, usually at and changes in auxin transport (Lopez-Bucio et al., 2002; Jain the expense of shoot growth (Kutz et al., 2002). Sulphate- et al., 2007). Low phosphate resistant (lpr) mutants of BIG, a deficient roots elongate faster than those with sufficient protein required for wild type levels of auxin transport, have sulphate, with LRs developing earlier, closer to the root tip reduced LRs in low Pi (Gil et al., 2001; Lopez-Bucio et al., and at a greater density (Kutz et al., 2002). This leads to an 2005). However, neither BIG nor auxin transport is required increase in total root surface area and a greater exploration of for other RSA modifications seen in low Pi (Lopez-Bucio the soil. et al., 2005). Interestingly, many root responses to phosphate Sulphur deprivation leads to transcriptional activation of starvation are repressed by cytokinin signalling (Franco-Zorrilla NITRILASE3 (NIT3), which converts indole-3-acetonitrile

(IAN) to auxin (Kutz et al., 2002). Low sulphate-induced 2005; Xiong et al., 2006). This is likely to be an adaptive LRPs exhibit high NIT3 promoter activity, thus generating response encouraging increased water uptake from deeper soil additional auxin close to the pericycle, allowing increased LR layers. The molecular mechanisms underpinning the response initiation (Kutz et al., 2002). Sulphur deficiency also upregulates are largely unknown, although ABA has an important role. the sulphate transporter genes SULTR1;1 and SULTR1;2 in The ABA-deficient mutants aba2-1 and aba3-2 have increased the epidermis and cortex of roots (Yoshimoto et al., 2002); both root system size compared with wild type under high osmotica transporters are reversibly downregulated in sulphate-replete (Deak & Malamy, 2005). Plants mutant for the LATERAL conditions (Maruyama-Nakashita et al., 2004). A sulphur ROOT DEVELOPMENT 2 (LRD2) and Arabidopsis response regulatory element (SURE) is conserved in the CYTPOLASMIC INVERTASE (AtCYT-INV1) genes also upstream region of a variety of sulphate-deficient response have a similar phenotype (Deak & Malamy, 2005; Qi et al., genes, suggesting that RSA alterations in response to sulphur 2007). Alongside ABA, LRD2 may be required to determine levels are coordinately controlled in Arabidopsis roots the percentage of LRPs that become LRs under normal and (Maruyama-Nakashita et al., 2004). stress conditions (Deak & Malamy, 2005). Interestingly, SURE regions contain ARF consensus Abscisic acid and drought stress have similar and probably sequences, suggesting a role for auxin in the early sulphate- synergistic effects on LR development. Several drought inhibition starvation response (Maruyama-Nakashita et al., 2004). A of lateral root growth (dig) mutants have enhanced responses to number of AUX/IAA genes have been implicated in the sul- ABA and are also drought tolerant, whilst others have a phate response, and transcriptomic analysis suggests that both reduced LR-inhibition response to ABA and are drought auxin influx and IAA28 activity may modulate the response to sensitive (Xiong et al., 2006). DIG3 is particularly important low sulphate, perhaps by acting in a negative regulatory manner for LR inhibition in response to ABA: dig3 mutants have (Nikiforova et al., 2003, 2005). More recently, (Dan et al., normal LR growth under stress and are susceptible to drought. 2007) suggested that auxin is involved in a subset of sulphur- Interestingly, dig3 plants were smaller than wild-type plants deficiency responses, with other hormones (such as cytokinin under well-watered conditions, suggesting that the ABA and and ABA) also playing a role. SULTR1 mRNA accumulation drought response involves factors required more generally for can be reduced by exogenous cytokinin, further suggesting growth (Xiong et al., 2006). Drought tolerance in crop species points of regulation (Maruyama-Nakashita et al., 2004). is controlled by multiple QTLs (Nguyen et al., 2004): it will be interesting to discover whether dig loci define drought- tolerant QTLs that are important for responding to water-stress 4. Potassium and lateral root development in roots and globally. Lateral roots of potassium-starved plants arrest their elongation (Armengaud et al., 2004). Analysis of root transcriptomes Salt stress Salt stress, which is related to drought stress, also from potassium-starved seedlings which were then resupplied reprograms RSA. Salt stress in Arabidopsis can induce root with potassium revealed that certain genes were downregulated swelling with shorter total root lengths, a seriously reduced by potassium resupply, including stress-induced genes, meristematic zone and a strong reduction in the number of transporters, calcium signalling components, sulphur LRPs, accompanied by the downregulation of several cell cycle metabolism components, and cell wall-remodelling enzymes. genes (Burssens et al., 2000). However, salt stress may also Conversely, upregulated genes were either transporters trigger an increase in LR number. In chickpea (Cicer arietinum), (including three root-specific nitrate transporters) or cell wall- the CAP2 (C. arietinum AP2) transcription factor is induced remodelling enzymes. The transcriptomic profile of potassium- upon dehydration and binds to dehydration-response elements starved plants overlaps with sulphur starvation, but not with in many stress-inducible genes (Boominathan et al., 2004; nitrate starvation or phosphate starvation, and also involves Shukla et al., 2006). Transgenic tobacco expressing CAP2 is changes in jasmonate/defence signalling (Armengaud et al., tolerant to salinity and osmotic stress, possibly because of a 2004). Interestingly, the MYB77 transcription factor provides large increase in LR number (Shukla et al., 2006). Many a direct link between potassium starvation responses and auxin-response genes associated with LR development are auxin signalling (Shin et al., 2007). upregulated in these plants, indicating links between salt stress responses and intrinsic auxin-associated development (Shukla et al., 2006). 5. Water and salt stresses He et al. (2005) reported increased LR numbers and a Water stress Water availability has a profound effect on a reduction of PR length in response to high levels of NaCl in plant’s root system. Plant roots will grow towards wetter soil Arabidopsis. The NAC2 transcription factor is upregulated by and away from high osmolarity (Takahashi et al., 2003). As NaCl and its overexpression causes increased LR formation water availability decreases (or osmotic stress increases), LR specifically without a change in root length (He et al., 2005). emergence is repressed, although LR initiation is largely NAC2 is upregulated by ethylene, auxin and ABA, and its unaffected (van der Weele et al., 2000; Deak & Malamy, induction by salt is compromised in auxin and ethylene

New Phytologist (2008) 179: 595–614 www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley revie w Review 607 signalling mutants (He et al., 2005). These data highlight the 7. Modulation of root architecture by biotic factors importance of phytohormone signalling in RSA responses to salinity. Within the soil, plants must compete and interact with a plethora of organisms, including microorganisms and other plant root systems. Roots secrete chemicals into the soil that 6. Effects of light on root architecture affect other plant RSAs and also influence communication Responding to light is key to plant survival. In addition to with microorganisms (Bais et al., 2004). In turn, viruses, having profound effects on the seed and shoot, light can affect bacteria and fungi can modify RSA. Many of these interacting LR morphology. This can be direct (e.g. red light enhances LR species are pathogens and result in plant defence responses, formation via the COL3 gene) (Datta et al., 2006) or indirect, while some can form symbiotic interactions leading to the via effects in the shoot (Bhalerao et al., 2002). formation of root nodules or mycorrhizas/proteoid roots The bZIP transcription factor LONG HYPOCOTYL 5 (Autran et al., 2006; Oldroyd & Downie, 2006). In addition, (HY5) is a key player in light-induced development in Arabi- soil microorganisms can produce auxin and cytokinin that dopsis (Koornneef et al., 1980). Initially noted for defective dramatically affect RSA (see Section III) (Costacurta & light-induced hypocotyl elongation, hy5 mutants also have an Vanderleyden, 1995). Some recent advances in the molecular elevated number of LRs, which grow faster than wild-type understanding of how pathogens modify RSA are presented roots and are less responsive to gravity (Oyama et al., 1997). in the following sections. The hy5 root phenotype occurs as a result of the underexpression of two negative regulators of the auxin signalling pathway: Viral proteins Cucumber mosaic virus (CMV) infects a range AUXIN RESISTANT 2 (AXR2)/IAA7 and SOLITARY of dicots, inducing developmental and growth abnormalities. ROOT (SLR)/IAA14 (see section III.1 ‘Lateral root initiation The severity of disease symptoms is dependent on the requires auxin and regulated protein degradation’; Cluis et al., CMV-2b protein (Lewsey et al., 2007). CMV-2b bypasses 2004). This interaction between HY5 and auxin signalling host defences both by inhibiting plant RNA silencing highlights the importance of both light-signalling networks mechanisms (thus promoting the undetected spread of viral and hormone-signalling networks in the control of RSA. HY5 RNA) and by antagonizing salicylic acid signalling, which also interacts with SALT TOLERANCE HOMOLOGUE 2 normally inhibits viral replication and cell-to-cell spreading. (STH2) (Datta et al., 2007). The sth2 mutant phenocopies Arabidopsis infected with CMV or overexpressing CMV-2b the exaggerated root phenotype of the hy5 mutant, and show perturbed RSA, specifically, shorter PRs, increased LR the authors suggest that light-dependent inhibition of LRs density and increased LR length, leading to increased root by STH2 requires its binding to HY5, where it provides surface area (Lewsey et al., 2007). Interestingly, CMV-2b transactivating potential to the transcription factor (Datta stabilizes a number of endogenous Arabidopsis mRNAs that et al., 2007). are targets of degradation by microRNAs (miRNAs), including HY5 HOMOLOGUE (HYH) is a functional equivalent of the auxin signalling genes ARF17 and NAC1. Curiously, HY5 with a similar expression pattern and responsiveness to stabilized ARF17 is proposed to inhibit LR formation (Mallory light (Sibout et al., 2006). hyh mutants show wild-type RSA. et al., 2005), whereas NAC1 promotes LR development (Xie However, hy5 hyh double mutants exhibit a suppression of et al., 2000), suggesting that targeting of NAC1 may be the hy5 phenotype, displaying less prolific root growth than particularly relevant during CMV infection. Cucumber wild type (Sibout et al., 2006). It has been proposed that mosaic virus ultimately inhibits root growth, but it is possible these double mutants represent the morphological response that transient increases in LR formation upon CMV infection to a quantitative gradient in auxin signalling. This example are advantageous during initial virus infection and spread, suggests that the inactivation of genes, both of which affect because the presence of a higher number of emerging LRs and the balance of a physiological process in the same manner, can an increase in root surface area could provide a greater number result in very different morphological changes (Sibout et al., of sites for virus entry. 2006). Molas et al (2006) examined total gene expression in Pathogenic bacteria and fungi Pathogenic bacteria and fungi dark-grown roots that were treated with red light for just 1 h. can directly influence LR development. Ralstonia solanacearum Interestingly, genes affecting cell wall metabolism and remod- inoculation leads to reduced formation and elongation of LRs elling were consistently downregulated. Genes involved in in petunia (Zolobowska & Van Gijsegem, 2006). Novel root hormone signalling (auxin, GA, ethylene) were also affected, lateral structures develop, derived from the pericycle founder as were proteins involved in intercellular transport, various cells that normally form LRs. These seem to act as colonization transcription factors and several F-box proteins (Molas et al., sites, and this process probably requires secreted bacterial 2006). Thus, light-induced changes in RSA are likely to proteins (Zolobowska & Van Gijsegem, 2006). happen rapidly and involve both signalling and remodelling The bacterium Pseudomonas syringae stimulates LR processes. development and other auxin-related changes in Arabidopsis,

whereas exogenous auxin promotes disease progression (Chen Specific cell types have been isolated from maize roots by et al., 2007). The authors suggest that auxin could promote laser capture microdissection (LCM) for transcriptomic cell wall loosening. A Pseudomonas peptide was reported to and proteomic analysis (Woll et al., 2005; Dembinsky et al., downregulate auxin signalling, enabling disease resistance; 2007). Comparison of the pericycle transcriptome of however, the effect on LR development was not investigated wild-type maize with that of a mutant that cannot initiate (Navarro et al., 2006). The rice transcription factor OsWRKY31 LRs revealed that the majority of differentially expressed is induced by rice blast fungus and also by auxin. Overexpression genes are involved in transcription or metabolism, or have of OsWRKY31 confers resistance to rice blast fungus infection unknown function. However, several genes involved in signal and also inhibits LR formation (Zhang et al., 2007b) In addition, transduction (especially protein kinases), cell cycle regulation, OsWRKY31 upregulates auxin responsive genes, again linking cellular transport and defence were also identified (Woll et al., auxin signalling and/or transport with the defence response 2005). (Zhang et al., 2007b). To identify genes involved in pericycle cell fate specification, Interestingly, the nitrate-inhibitory effect on LR development rather than LR formation per se, pericycle cells were dissected is over-ridden when plants are inoculated with Phyllobacterium, from along the length of the root before the time that cell a growth-promoting rhizobacterium (Mantelin et al., 2006). divisions occur (Dembinsky et al., 2007). The pericycle This effect was accompanied by altered expression of various transcriptome and proteome was analysed, and further transport genes, including AtNRT1.1. pericycle-enriched genes were isolated from cDNA libraries Continuing research in this new area will define the extent and expressed sequence tags (ESTs) (Dembinsky et al., 2007). to which plant–pathogen interactions affect RSA. Around 40 ‘pericycle-specific’ genes were identified, of which the largest two subsets were transcriptional regulators and unknown genes. Compared with vascular cells, pericycle V. Transcriptomic studies to identify potential appears enriched in genes involved in protein synthesis, but new regulators of lateral root development low in genes regulating cell fate. Twenty abundant soluble With the advent of high-throughput ‘omic’ experimental pericycle proteins were identified, of which 80% have a meta- techniques, it is possible to augment molecular genetic bolic or energy function. There is only a small overlap between studies of LR developmental mechanisms. This has included the LR initiation data set (Woll et al., 2005) and the pericycle the generation of data sets of genes that are upregulated data sets (Dembinsky et al., 2007), suggesting that specifying or downregulated specifically in different root cell types pericycle cell identity is a distinct process from forming a or in response to specific signals (see various sections new LR. above). In terms of probing cell type-specific gene expression in VI. Conclusions and future challenges roots, studies from the Benfey laboratory have been influential. An initial study identified several hundred genes enriched in A vast number of signals, both from within and outside the vascular tissues, including pericycle (Birnbaum et al., 2003). plant, impinge on the root to regulate its final architecture and More recently, a high-resolution gene-expression map of branching pattern. Many challenges still exist for future ‘root all root cell types, including pericycle, xylem pole pericycle, biologists’. We must understand at the molecular level how phloem pole pericycle and LRPs, has been created (Brady these different signals work together to direct pericycle cell et al., 2007). Analysis of this vast data set will provide new behaviour and later LR developmental processes. We must insights into the gene regulation occurring during LR discover potentially novel signals that regulate LR develop- development. For example, pericycle (in particular xylem pole mental proteins which currently reside outside known pericycle) is enriched in mRNAs encoding cell wall-modifying signalling networks. There are questions we can ask about the enzymes, whereas genes encoding kinases and enzymes required evolution of RSA regulation across the plant kingdom. There for cell wall loosening are enriched in LRPs. In addition, auxin are huge transcriptomic data sets that will provide us with new biosynthetic genes are enriched in pericycle and LRPs, and clues about the changes in gene expression necessary for LR ABA signalling components are enriched in pericycle (Brady development to occur. Moving our knowledge gained in et al., 2007). Arabidopsis and genetically tractable crop plants into other A meta-analysis identifying indirect targets of the SHOR- agronomically relevant species will provide an understanding TROOT (SHR) transcription factor uncovered a number of of how to engineer crop plants that can exist in a range of SHR-regulated genes that were enriched in or exclusive to potentially problematic environments. pericycle (Levesque et al., 2006). It is thus tempting to specu- late that SHR signalling pathways may regulate LR formation Acknowledgements as well as PR development (Scheres et al., 2002), especially as similar signalling may regulate AR formation in pine trees and The authors thank Laurent Laplaze and Jeremy Roberts for sweet chestnut trees (Sanchez et al., 2007). useful comments.

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References 2004. The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 encodes a novel protein mediating abscisic acid and sugar responses Armengaud P, Breitling R, Amtmann A. 2004. The potassium-dependent essential for growth. The Plant Cell 16: 406–421. transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in Burssens S, Himanen K, van de Cotte B, Beeckman T, Van Montagu M, nutrient signaling. Plant Physiology 136: 2556–2576. Inze D, Verbruggen N. 2000. Expression of cell cycle regulatory genes and Arnao MB, Hernandez-Ruiz J. 2007. Melatonin promotes adventitious- and morphological alterations in response to salt stress in Arabidopsis thaliana. lateral root regeneration in etiolated hypocotyls of Lupinus albus L. Journal Planta 211: 632–640. of Pineal Research 42: 147–152. Caba JM, Centeno ML, Fernandez B, Gresshoff PM, Ligero F. 2000. Autran D, Laplaze L, Hocher V, Auguy F, Oureye-Sy M, Obertello M, Inoculation and nitrate alter phytohormone levels in soybean roots: Péret B, Franche C, Bogusz D. 2006. Make your way to nodules. Early differences between a supernodulating mutant and the wild type. events in actinorhizal and legumes nitrogen fixing symbioses. In: Planta 211: 98–104. Hemantaranjan A, ed. Advances in Plant Physiology, vol. 9. Jodhpur, India: Cannon WA. 1949. A tentative classsification of root systems. Ecology Scientific Publishers, 327–344. 30: 542–548. Axtell MJ, Snyder JA, Bartel DP. 2007. Common functions for diverse small Carol RJ, Dolan L. 2002. Building a hair: tip growth in Arabidopsis thaliana RNAs of land plants. The Plant Cell 19: 1750–1769. root hairs. Philosophical Transactions of the Royal Society of London. Series B, Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM. 2004. How plants Biological Sciences 357: 815–821. communicate using the underground information superhighway. Trends Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, in Plant Science 9: 26–32. Sandberg G, Bennett MJ. 2003. Dissecting Arabidopsis lateral root Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z. 2004. development. Trends in Plant Science 8: 165–171. Brassinosteroids interact with auxin to promote lateral root development Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, in Arabidopsis. Plant Physiology 134: 1624–1631. Graham N, Inze D, Sandberg G, Casero PJ et al. 2001. Auxin transport Beeckman T, Burssens S, Inze D. 2001. The peri-cell-cycle in Arabidopsis. promotes Arabidopsis lateral root initiation. The Plant Cell 13: 843–852. Journal of Experimental Botany 52: 403–411. Casson SA, Lindsey K. 2003. Genes and signalling in root development. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens New Phytologist 156: 11–38. G, Friml J. 2003. Local, efflux-dependent auxin gradients as a common Celenza JLJ, Grisafi PL, Fink GR. 1995. A pathway for lateral root module for plant organ formation. Cell 115: 591–602. formation in Arabidopsis thaliana. Genes & Development 9: 2131–2142. Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G. 2002. Chen CW, Yang YW, Lur HS, Tsai YG, Chang MC. 2006a. A novel Shoot-derived auxin is essential for early lateral root emergence in function of abscisic acid in the regulation of rice (Oryza sativa L.) root Arabidopsis seedlings. Plant Journal 29: 325–332. growth and development. Plant & Cell Physiology 47: 1–13. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith Chen JG, Gao Y, Jones AM. 2006b. Differential roles of Arabidopsis DW, Benfey PN. 2003. A gene expression map of the Arabidopsis root. heterotrimeric G-protein subunits in modulating cell division in roots. Science 302: 1956–1960. Plant Physiology 141: 887–897. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN. 2007. Aida M, Palme K, Scheres B. 2005. The PIN auxin efflux facilitator Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana network controls growth and patterning in Arabidopsis roots. Nature auxin physiology. Proceedings of the National Academy of Sciences, USA 104: 433: 39–44. 20131–20136. Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Cheng JC, Lertpiriyapong K, Wang S, Sung ZR. 2000. The role of the Caboche M, Van Onckelen H, Van Montagu M, Inze D. 1995. Arabidopsis ELD1 gene in cell development and photomorphogenesis in Superroot, a recessive mutation in Arabidopsis, confers auxin darkness. Plant Physiology 123: 509–520. overproduction. The Plant Cell 7: 1405–1419. Cheng JC, Seeley KA, Sung ZR. 1995. RML1 and RML2, Arabidopsis Bonser AM, Lynch J, Snapp S. 1996. Effect of phosphorus deficiency on genes required for cell proliferation at the root tip. Plant Physiology growth angle of basal roots in Phaseolus vulgaris. New Phytologist 132: 107: 365–376. 281–288. Chuang HW, Zhang W, Gray WM. 2004. Arabidopsis ETA2, an apparent Boominathan P, Shukla R, Kumar A, Manna D, Negi D, Verma PK, ortholog of the human cullin-interacting protein CAND1, is required for Chattopadhyay D. 2004. Long term transcript accumulation during auxin responses mediated by the SCF(TIR1) ubiquitin ligase. The Plant the development of dehydration adaptation in Cicer arietinum. Plant Cell 16: 1883–1897. Physiology 135: 1608–1620. Cluis CP, Mouchel CF, Hardtke CS. 2004. The Arabidopsis transcription Bostick M, Lochhead SR, Honda A, Palmer S, Callis J. 2004. Related to factor HY5 integrates light and hormone signaling pathways. ubiquitin 1 and 2 are redundant and essential and regulate vegetative Plant Journal 38: 332–347. growth, auxin signaling, and ethylene production in Arabidopsis. The Coates JC, Laplaze L, Haseloff J. 2006. Armadillo-related proteins promote Plant Cell 16: 2418–2432. lateral root development in Arabidopsis. Proceedings of the National Boukcim H, Pages L, Mousain D. 2006. Local NO3− or NH4+ supply Academy of Sciences, USA 103: 1621–1626. modifies the root system architecture of Cedrus atlantica seedlings grown Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L. 2006. in a split-root device. Journal of Plant Physiology 163: 1293–1304. Nitric oxide modulates the expression of cell cycle regulatory genes Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, during lateral root formation in tomato. Journal of Experimental Botany Ohler U, Benfey PN. 2007. A high-resolution root spatiotemporal map 57: 581–588. reveals dominant expression patterns. Science 318: 801–806. Costacurta A, Vanderleyden J. 1995. Synthesis of phytohormones by Brady SM, Sarkar SF, Bonetta D, McCourt P. 2003. The ABSCISIC ACID plant-associated bacteria. Critical Reviews in Microbiology 21: 1–18. INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is Dan H, Yang G, Zheng ZL. 2007. A negative regulatory role for auxin in involved in auxin signaling and lateral root development in Arabidopsis. sulphate deficiency response in Arabidopsis thaliana. Plant Molecular Plant Journal 34: 67–75. Biology 63: 221–235. Bright LJ, Liang Y, Mitchell DM, Harris JM. 2005. The LATD gene of Datta S, Hettiarachchi C, Johansson H, Holm M. 2007. SALT Medicago truncatula is required for both nodule and root development. TOLERANCE HOMOLOG2, a B-box protein in Arabidopsis that Molecular Plant–Microbe Interactions 18: 521–532. activates transcription and positively regulates light-mediated Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR. development. The Plant Cell 19: 3242–3255.

Datta S, Hettiarachchi GH, Deng XW, Holm M. 2006. Arabidopsis Dubrovsky JG, Gambetta GA, Hernandez-Barrera A, Shishkova S, CONSTANS-LIKE3 is a positive regulator of red light signaling and root Gonzalez I. 2006. Lateral root initiation in Arabidopsis: developmental growth. The Plant Cell 18: 70–84. window, spatial patterning, density and predictability. Annals of Botany De Smet I, Jurgens G. 2007. Patterning the axis in plants – auxin in control. 97: 903–915. Current Opinion in Genetics & Development 17: 337–343. Dubrovsky JG, Rost TL. 2005. Pericycle. In: Roberts KR, ed. Encyclopaedia De Smet I, Signora L, Beeckman T, Inze D, Foyer CH, Zhang H. 2003. An of life sciences. Chichester, UK: John Wiley and Sons Ltd, doi: 10.1038/ abscisic acid-sensitive checkpoint in lateral root development of npg.els.0002085. Arabidopsis. Plant Journal 33: 543–555. Echevarria-Machado I, Escobedo-G MRM, Larque-Saavedra A. 2007. De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Responses of transformed Catharanthus roseus roots to femtomolar Swarup R, Naudts M, Vanneste S, Audenaert D et al. 2007. concentrations of salicylic acid. Plant Physiology and Biochemistry Auxin-dependent regulation of lateral root positioning in the basal 45: 501–507. meristem of Arabidopsis. Development 134: 681–690. Fitter A, Williamson L, Linkohr B, Leyser O. 2002. Root system De Smet I, Vanneste S, Inze D, Beeckman T. 2006a. Lateral root initiation architecture determines fitness in an Arabidopsis mutant in competition or the birth of a new meristem. Plant Molecular Biology 60: 871–887. for immobile phosphate ions but not for nitrate ions. Proceedings Biological De Smet I, Zhang H, Inze D, Beeckman T. 2006b. A novel role for Sciences 269: 2017–2022. abscisic acid emerges from underground. Trends in Plant Science de Folter S, Immink RG, Kieffer M, Parenicova L, Henz SR, Weigel D, 11: 434–439. Busscher M, Kooiker M, Colombo L, Kater MM et al. 2005. De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, Comprehensive interaction map of the Arabidopsis MADS Box van der Schueren E, Maes S, Naudts M, Inze D. 2001. Functional transcription factors. The Plant Cell 17: 1424–1433. analysis of cyclin-dependent kinase inhibitors of Arabidopsis. The Plant Franco-Zorrilla JM, Martin AC, Leyva A, Paz-Ares J. 2005. Interaction Cell 13: 1653–1668. between phosphate-starvation, sugar, and cytokinin signaling in De Veylder L, Beeckman T, Inze D. 2007. The ins and outs of the plant cell Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 cycle. Nature Reviews. Molecular Cell Biology 8: 655–665. and AHK3. Plant Physiology 138: 847–857. Deak KI, Malamy J. 2005. Osmotic regulation of root system architecture. Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M. 2005. Plant Journal 43: 17–28. Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk LA, Lamkemeyer alters lateral root development in Arabidopsis. Plant Journal 44: T, Fladerer C, Madlung J, Barbazuk B et al. 2007. Transcriptomic and 382–395. proteomic analyses of pericycle cells of the maize primary root. Plant Fukaki H, Okushima Y, Tasaka M. 2007. Auxin-mediated lateral Physiology 145: 575–588. root formation in higher plants. International Review of Cytology 256: Devaiah BN, Karthikeyan AS, Raghothama KG. 2007. WRKY75 111–137. transcription factor is a modulator of phosphate acquisition and root Fukaki H, Tameda S, Masuda H, Tasaka M. 2002. Lateral root formation development in Arabidopsis. Plant Physiology 143: 1789–1801. is blocked by a gain-of-function mutation in the SOLITARY-ROOT/ Dharmasiri N, Dharmasiri S, Estelle M. 2005a. The F-box protein TIR1 is IAA14 gene of Arabidopsis. Plant Journal 29: 153–168. an auxin receptor. Nature 435: 441–445. Fukaki H, Taniguchi N, Tasaka M. 2006. PICKLE is required for Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 Ehrismann JS, Jurgens G, Estelle M. 2005b. Plant development is activity during Arabidopsis lateral root initiation. Plant Journal regulated by a family of auxin receptor F box proteins. Developmental Cell 48: 380–389. 9: 109–119. Gan Y, Filleur S, Rahman A, Gotensparre S, Forde BG. 2005. Nutritional DiDonato RJ, Arbuckle E, Buker S, Sheets J, Tobar J, Totong R, regulation of ANR1 and other root-expressed MADS-box genes in Grisafi P, Fink GR, Celenza JL. 2004. Arabidopsis ALF4 encodes a Arabidopsis thaliana. Planta 222: 730–742. nuclear-localized protein required for lateral root formation. Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, Palme K, Estelle Plant Journal 37: 340–353. M, Chory J. 2001. BIG: a calossin-like protein required for polar auxin Dittmer HJ. 1937. A quantitative study of the roots and root hairs of a winter transport in Arabidopsis. Genes & Development 15: 1985–1997. rye plant (Secale cereale). American Journal of Botany 24: 417–420. Gonzalez-Carranza ZH, Elliott KA, Roberts JA. 2007. Expression of Dolan L, Costa S. 2001. Evolution and genetics of root hair stripes in the polygalacturonases and evidence to support their role during cell root epidermis. Journal of Experimental Botany 52: 413–417. separation processes in Arabidopsis thaliana. Journal of Experimental Botany Dong L, Wang L, Zhang Y, Zhang Y, Deng X, Xue Y. 2006. An 58: 3719–3730. auxin-inducible F-box protein CEGENDUO negatively regulates Gonzalez-Rizzo S, Crespi M, Frugier F. 2006. The Medicago truncatula auxin-mediated lateral root formation in Arabidopsis. Plant Molecular CRE1 cytokinin receptor regulates lateral root development and early Biology 60: 599–615. symbiotic interaction with Sinorhizobium meliloti. The Plant Cell de Dorlodot S, Forster B, Pages L, Price A, Tuberosa R, Draye X. 2007. 18: 2680–2693. Root system architecture: opportunities and constraints for genetic Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M. 2001. Auxin improvement of crops. Trends in Plant Science 12: 474–481. regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Dreher KA, Brown J, Saw RE, Callis J. 2006. The Arabidopsis Aux/IAA Nature 414: 271–276. protein family has diversified in degradation and auxin responsiveness. Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, The Plant Cell 18: 699–714. Crosby WL, Yang M, Ma H, Estelle M. 1999. Identification of an Drew MC. 1975. Comparison of the effects of a localised supply of SCF ubiquitin-ligase complex required for auxin response in Arabidopsis phosphate, nitrate, ammonium and potassium on the growth thaliana. Genes & Development 13: 1678–1691. of the seminal root system, and the shoot, in barley. New Phytologist Hamada S, Ezaki S, Hayashi K, Toko K, Yamafuji K. 1992. Electric Current 75: 79–90. Precedes Emergence of a Lateral Root in Higher Plants. Plant Physiology Drew MC, Saker LR. 1975. Nutrient supply and the growth of the 100: 614–619. seminal root system of barley. II. Localized, compensatory increases in He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY. 2005. AtNAC2, lateral root growth and rates of nitrate uptake when nitrate supply is a transcription factor downstream of ethylene and auxin signaling restricted to only part of the root system. Journal of Experimental Botany pathways, is involved in salt stress response and lateral root development. 26: 79–90. Plant Journal 44: 903–916.

New Phytologist (2008) 179: 595–614 www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley revie w Review 611

Hellmann H, Hobbie L, Chapman A, Dharmasiri S, Dharmasiri N, del D, Calvo V, Parizot B, Herrera-Rodriguez MB et al. 2007. Cytokinins act Pozo C, Reinhardt D, Estelle M. 2003. Arabidopsis AXR6 encodes CUL1 directly on lateral root founder cells to inhibit root initiation. The Plant implicating SCF E3 ligases in auxin regulation of embryogenesis. Cell 19: 3889–3900. The EMBO Journal 22: 3314–3325. Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R. 2006. Expression Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inze D, profiling of auxin-treated Arabidopsis roots: toward a molecular analysis Beeckman T. 2002. Auxin-mediated cell cycle activation during early of lateral root emergence. Plant & Cell Physiology 47: 788–792. lateral root initiation. The Plant Cell 14: 2339–2351. Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM. 1995. Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Formation of lateral root meristems is a two-stage process. Chriqui D, Van Montagu M, Inze D, Beeckman T. 2004. Tra nsc ri p t Development 121: 3303–3310. profiling of early lateral root initiation. Proceedings of the National Academy Lelandais-Briere C, Jovanovic M, Torres GA, Perrin Y, Lemoine R, of Sciences, USA 101: 5146–5151. Corre-Menguy F, Hartmann C. 2007. Disruption of AtOCT1, Hirota A, Kato T, Fukaki H, Aida M, Tasaka M. 2007. The an organic cation transporter gene, affects root development and auxin-regulated AP2/EREBP gene PUCHI is required for carnitine-related responses in Arabidopsis. Plant Journal 51: 154–164. morphogenesis in the early lateral root primordium of Arabidopsis. Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, Hassan H, The Plant Cell 19: 2156–2168. Nakajima K, Matsumoto N, Lohmann JU et al. 2006. Whole-genome Hochholdinger F, Park WJ, Sauer M, Woll K. 2004. From weeds to crops: analysis of the SHORT-ROOT developmental pathway in Arabidopsis. genetic analysis of root development in cereals. Trends in Plant Science PLoS Biology 4: e143. 9: 42–48. Lewsey M, Robertson FC, Canto T, Palukaitis P, Carr JP. 2007. Hochholdinger F, Zimmermann R. 2008. Conserved and diverse Selective targeting of miRNA-regulated plant development by a viral mechanisms in root development. Current Opinion in Plant Biology counter-silencing protein. Plant Journal 50: 240–252. 11: 70–74. Li J, Zhu S, Song X, Shen Y, Chen H, Yu J, Yi K, Liu Y, Karplus VJ, Wu P Hou G, Hill JP, Blancaflor EB. 2004. Developmental anatomy and auxin et al. 2006a. A rice glutamate receptor-like gene is critical for the division response of lateral root formation in Ceratopteris richardii. Journal of and survival of individual cells in the root apical meristem. The Plant Cell Experimental Botany 55: 685–693. 18: 340–349. Ivanchenko MG, Coffeen WC, Lomax TL, Dubrovsky JG. 2006. Li X, Mo X, Shou H, Wu P. 2006b. Cytokinin-mediated cell cycling arrest Mutations in the Diageotropica (Dgt) gene uncouple patterned cell of pericycle founder cells in lateral root initiation of Arabidopsis. Plant & division during lateral root initiation from proliferative cell division Cell Physiology 47: 1112–1123. in the pericycle. Plant Journal 46: 436–447. Liang Y, Harris JM. 2005. Response of root branching to abscisic acid is Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miege C, Gaude T. correlated with nodule formation both in legumes and nonlegumes. 2007. The retromer protein VPS29 links cell polarity and organ initiation American Journal of Botany 92: 1675–1683. in plants. Cell 130: 1057–1070. Liang Y, Mitchell DM, Harris JM. 2007. Abscisic acid rescues the root Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, meristem defects of the Medicago truncatula latd mutant. Development Titapiwatanakun B, Murphy AS, Raghothama KG. 2007. Differential Biology 304: 297–307. effects of sucrose and auxin on localized phosphate deficiency-induced Linkohr BI, Williamson LC, Fitter AH, Leyser HM. 2002. Nitrate and modulation of different traits of root system architecture in Arabidopsis. phosphate availability and distribution have different effects on root Plant Physiology 144: 232–247. system architecture of Arabidopsis. Plant Journal 29: 751–760. Jiang C, Gao X, Liao L, Harberd NP, Fu X. 2007. Phosphate Starvation Little DY, Rao H, Oliva S, Daniel-Vedele F, Krapp A, Malamy JE. 2005. Root Architecture and Anthocyanin Accumulation Responses Are The putative high-affinity nitrate transporter NRT2.1 represses lateral root Modulated by the Gibberellin-DELLA Signaling Pathway in Arabidopsis. initiation in response to nutritional cues. Proceedings of the National Plant Physiology 145: 1460–1470. Academy of Sciences, USA 102: 13693–13698. Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim WY, Van Oosten M, Hyun Liu KH, Huang CY, Tsay YF. 1999. CHL1 is a dual-affinity nitrate Y, Somers DE, Lee I et al. 2008. The SUMO E3 ligase, AtSIZ1, regulates transporter of Arabidopsis involved in multiple phases of nitrate uptake. flowering by controlling a salicylic acid-mediated floral promotion The Plant Cell 11: 865–874. pathway and through affects on FLC chromatin structure. Plant Journal Liu W, Xu ZH, Luo D, Xue HW. 2003. Roles of OsCKI1, a rice casein 53: 530–540. kinase I, in root development and plant hormone sensitivity. Plant Journal Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, 36: 189–202. Raghothama KG. 2007. Phosphate starvation responses are Lopez-Bucio J, Acevedo-Hernandez G, Ramirez-Chavez E, Molina-Torres mediated by sugar signaling in Arabidopsis. Planta 225: 907–918. J, Herrera-Estrella L. 2006. Novel signals for plant development. Current Kepinski S, Leyser O. 2005. The Arabidopsis F-box protein TIR1 is an auxin Opinion in Plant Biology 9: 523–529. receptor. Nature 435: 446–451. Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo Koiwai H, Tagiri A, Katoh S, Katoh E, Ichikawa H, Minami E, Nishizawa MF, Simpson J, Herrera-Estrella L. 2002. Phosphate availability alters Y. 2007. RING-H2 type ubiquitin ligase EL5 is involved in root architecture and causes changes in hormone sensitivity in the Arabidopsis development through the maintenance of cell viability in rice. root system. Plant Physiology 129: 244–256. Plant Journal 51: 92–104. Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-Torres A, Kolbert Z, Bartha B, Erdei L. 2007. Exogenous auxin-induced NO synthesis Rampey RA, Bartel B, Herrera-Estrella L. 2005. An auxin transport is nitrate reductase-associated in Arabidopsis thaliana root primordia. independent pathway is involved in phosphate stress-induced root Journal of Plant Physiology, doi: 10.1016/j.jplph.2007.07.019 architectural alterations in Arabidopsis. Identification of BIG as a Koornneef M, Rolff E, Spruiy CJP. 1980. Genetic control of light inhibited mediator of auxin in pericycle cell activation. Plant Physiology hypocotyl elongation in Arabidopsis thaliana. Pflanzenphysiologie 100: 137: 681–691. 147–160. Lopez-Bucio J, Millan-Godinez M, Mendez-Bravo A, Morquecho- Kutz A, Muller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW. Contreras A, Ramirez-Chavez E, Molina-Torres J, Perez-Torres A, 2002. A role for nitrilase 3 in the regulation of root morphology in Higuchi M, Kakimoto T, Herrera-Estrella L. 2007. Cytokinin receptors sulphur-starving Arabidopsis thaliana. Plant Journal 30: 95–106. are involved in alkamide regulation of root and shoot development in Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers Arabidopsis. Plant Physiology 145: 1703–1713.

Lopez-Bucio J, Nieto-Jacobo MF, Ramirez-Rodriguez VV, Herrera-Estrella deciphers informational fluxes of sulphur stress response. Journal of L. 2000. Organic acid metabolism in plants: from adaptive physiology Experimental Botany 56: 1887–1896. to transgenic varieties for cultivation in extreme soils. Plant Science Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY. 2004. 160: 1–13. The ubiquitin ligase XBAT32 regulates lateral root development in Loudet O, Gaudon V, Trubuil A, Daniel-Vedele F. 2005. Quantitative Arabidopsis. Plant Journal 40: 996–1006. trait loci controlling root growth and architecture in Arabidopsis Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. 2007. ARF7 thaliana confirmed by heterogeneous inbred family. Theoretical and ARF19 regulate lateral root formation via direct activation of LBD/ and Applied Genetics 110: 742–753. ASL genes in Arabidopsis. The Plant Cell 19: 118–130. Lucas M, Godin C, Jay-Allemand C, Laplaze L. 2007. Auxin fluxes in the Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, root apex co-regulate gravitropism and lateral root initiation. Journal of Ecker JR, Hughes B, Lui A, Nguyen D et al. 2005. Functional genomic Experimental Botany 59: 56–66. analysis of the AUXIN RESPONSE FACTOR gene family members in Malamy JE, Benfey PN. 1997. Organization and cell differentiation in Arabidopsis thaliana: unique and overlapping functions of ARF7 and lateral roots of Arabidopsis thaliana. Development 124: 33–44. ARF19. The Plant Cell 17: 444–463. Malamy JE, Ryan KS. 2001. Environmental regulation of lateral root Oldroyd GE, Downie JA. 2004. Calcium, kinases and nodulation signalling initiation in Arabidopsis. Plant Physiology 127: 899–909. in legumes. Nature Reviews. Molecular Cell Biology 5: 566–576. Mallory AC, Bartel DP, Bartel B. 2005. MicroRNA-directed regulation Oldroyd GE, Downie JA. 2006. Nuclear calcium changes at the core of of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper symbiosis signalling. Current Opinion in Plant Biology 9: 351–357. development and modulates expression of early auxin response genes. Osmont KS, Sibout R, Hardtke CS. 2007. Hidden branches: The Plant Cell 17: 1360–1375. developments in root system architecture. Annual Review of Plant Biology Mantelin S, Desbrosses G, Larcher M, Tranbarger TJ, Cleyet-Marel JC, 58: 93–113. Touraine B. 2006. Nitrate-dependent control of root architecture and Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Hughes B, Liu A, Onodera C, Quach H et al. 2005. Functional genomic Planta 223: 591–603. analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H. 2004. members in Arabidopsis thaliana. The Plant Cell 17: 3282–3300. Regulation of high-affinity sulphate transporters in plants: towards Oyama T, Shimura Y, Okada K. 1997. The Arabidopsis HY5 gene encodes systematic analysis of sulphur signalling and regulation. Journal of a bZIP protein that regulates stimulus-induced development of root and Experimental Botany 55: 1843–1849. hypocotyl. Genes & Development 11: 2983–2995. Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso Parizot B, Laplaze L, Ricaud L, Boucheron-Dubuisson E, Bayle V, Bonke JM, Ecker JR, Schaller GE. 2005. Multiple type-B response regulators M, De Smet I, Poethig SR, Helariutta Y, Haseloff J et al. 2008. Diarch mediate cytokinin signal transduction in Arabidopsis. The Plant Cell symmetry of the vascular bundle in Arabidopsis root encompasses the 17: 3007–3018. pericycle and is reflected in distich lateral root initiation. Plant Physiology Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer 146: 140–148. DG, Dolan L. 2007. An ancient mechanism controls the development Petroski MD, Deshaies RJ. 2005. Function and regulation of of cells with a rooting function in land plants. Science 316: 1477–1480. cullin-RING ubiquitin ligases. Nature Reviews. Molecular Cell Biology Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, 6: 9–20. Baek D, Koo YD, Jin JB, Bressan RA et al. 2005. The Arabidopsis del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C. 2006. The balance SUMO E3 ligase SIZ1 controls phosphate deficiency responses. between cell division and endoreplication depends on E2FC-DPB, Proceedings of the National Academy of Sciences, USA 102: transcription factors regulated by the ubiquitin-SCFSKP2A pathway in 7760–7765. Arabidopsis. The Plant Cell 18: 2224–2235. Molas ML, Kiss JZ, Correll MJ. 2006. Gene profiling of the red light Qi X, Wu Z, Li J, Mo X, Wu S, Chu J, Wu P. 2007. AtCYT-INV1, a neutral signalling pathways in roots. Journal of Experimental Botany 57: invertase, is involved in osmotic stress-induced inhibition on lateral root 3217–3229. growth in Arabidopsis. Plant Molecular Biology 64: 575–587. Munos S, Cazettes C, Fizames C, Gaymard F, Tillard P, Lepetit M, Lejay Raghothama KG. 1999. Phosphate acquisition. Annual Review of Plant L, Gojon A. 2004. Transcript profiling in the chl1-5 .mutant of Physiology and Plant Molecular Biology 50: 665–693. Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the Ramirez-Chavez E, Lopez-Bucio J, Herrera-Estrella L, Molina-Torres J. regulation of another nitrate transporter, NRT2.1. The Plant Cell 2004. Alkamides isolated from plants promote growth and alter root 16: 2433–2447. development in Arabidopsis. Plant Physiology 134: 1058–1068. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet Rani Debi B, Taketa S, Ichii M. 2005. Cytokinin inhibits lateral root O, Jones JD. 2006. A plant miRNA contributes to antibacterial resistance initiation but stimulates lateral root elongation in rice (Oryza sativa). by repressing auxin signaling. Science 312: 436–439. Journal of Plant Physiology 162: 507–515. Neuteboom LW, Ng JM, Kuyper M, Clijdesdale OR, Hooykaas PJ, van der Razem FA, El-Kereamy A, Abrams SR, Hill RD. 2006. The RNA-binding Zaal BJ. 1999. Isolation and characterization of cDNA clones protein FCA is an abscisic acid receptor. Nature 439: 290–294. corresponding with mRNAs that accumulate during auxin-induced lateral Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, Gojon A. root formation. Plant Molecular Biology 39: 273–287. 2006. A central role for the nitrate transporter NRT2.1 in the integrated Nguyen TT, Klueva N, Chamareck V, Aarti A, Magpantay G, Millena AC, morphological and physiological responses of the root system to nitrogen Pathan MS, Nguyen HT. 2004. Saturation mapping of QTL regions and limitation in Arabidopsis. Plant Physiology 140: 909–921. identification of putative candidate genes for drought tolerance in rice. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Molecular Genetics and Genomics 272: 35–46. Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y et al. 2008. The Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R. 2003. Physcomitrella genome reveals evolutionary insights into the conquest of Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: land by plants. Science 319: 64–69. interlacing of biosynthetic pathways provides response specificity. Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T. 2006. Plant Journal 33: 633–650. Identification of QTL controlling root growth response to phosphate Nikiforova VJ, Daub CO, Hesse H, Willmitzer L, Hoefgen R. 2005. starvation in Arabidopsis thaliana. Plant, Cell & Environment Integrative gene-metabolite network with implemented causality 29: 115–125.

New Phytologist (2008) 179: 595–614 www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley revie w Review 613

Riefler M, Novak O, Strnad M, Schmulling T. 2006. Arabidopsis cytokinin Soucek P, Klima P, Rekova A, Brzobohaty B. 2007. Involvement of receptor mutants reveal functions in shoot growth, leaf senescence, seed hormones and KNOXI genes in early Arabidopsis seedling development. size, germination, root development, and cytokinin metabolism. Journal of Experimental Botany 58: 3797–3810. The Plant Cell 18: 40–54. Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM. 2005. A link Rogg LE, Lasswell J, Bartel B. 2001. A gain-of-function mutation between ethylene and auxin uncovered by the characterization of two in IAA28 suppresses lateral root development. The Plant Cell root-specific ethylene-insensitive mutants in Arabidopsis. The Plant Cell 13: 465–480. 17: 2230–2242. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, 2001. A conserved MYB transcription factor involved in phosphate Blanchet A, Nussaume L, Desnos T. 2007. Root tip contact with starvation signaling both in vascular plants and in unicellular algae. Genes low-phosphate media reprograms plant root architecture. Nature Genetics & Development 15: 2122–2133. 39: 792–796. Samaj J, Baluska F, Menzel D. 2004. New signalling molecules regulating Takahashi N, Yamazaki Y, Kobayashi A, Higashitani A, Takahashi H. 2003. root hair tip growth. Trends in Plant Science 9: 217–220. Hydrotropism interacts with gravitropism by degrading amyloplasts Sanchez C, Vielba JM, Ferro E, Covelo G, Sole A, Abarca D, de Mier BS, in seedling roots of Arabidopsis and radish. Plant Physiology 132: Diaz-Sala C. 2007. Two SCARECROW-LIKE genes are induced in 805–810. response to exogenous auxin in rooting-competent cuttings of distantly Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR. related forest species. Tree Physiolog y 27: 1459–1470. 2003. Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Cruz-Ramirez A, dioxygenase gene family. Plant Journal 35: 44–56. Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L. 2005. Phosphate Taramino G, Sauer M, Stauffer JLJ, Multani D, Niu X, Sakai H, starvation induces a determinate developmental program in the roots of Hochholdinger F. 2007. The maize (Zea mays L.) RTCS gene Arabidopsis thaliana. Plant & Cell Physiology 46: 174–184. encodes a LOB domain protein that is a key regulator of embryonic Sano T, Nagata T. 2002. The possible involvement of a phosphate-induced seminal and post-embryonic shoot-borne root initiation. transcription factor encoded by phi-2 gene from tobacco in ABA-signaling Plant Journal 50: 649–659. pathways. Plant & Cell Physiology 43: 12–20. Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova Liscum E, Yamamoto KT. 2004. MASSUGU2 encodes Aux/IAA19, an E. 2006. Canalization of auxin flow by Aux/IAA-ARF-dependent auxin-regulated protein that functions together with the transcriptional feedback regulation of PIN polarity. Genes & Development 20: activator NPH4/ARF7 to regulate differential growth responses of 2902–2911. hypocotyl and formation of lateral roots in Arabidopsis thaliana. Sawa S, Ohgishi M, Goda H, Higuchi K, Shimada Y, Yoshida S, Koshiba The Plant Cell 16: 379–393. T. 2002. The HAT2 gene, a member of the HD-Zip gene family, isolated Teale WD, Paponov IA, Palme K. 2006. Auxin in action: signalling, as an auxin inducible gene by DNA microarray screening, affects auxin transport and the control of plant growth and development. Nature response in Arabidopsis. Plant Journal 32: 1011–1022. Reviews. Molecular Cell Biology 7: 847–859. Scheres B. 2007. Stem-cell niches: nursery rhymes across kingdoms. Nature Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S. 2004. Arabidopsis Reviews. Molecular Cell Biology 8: 345–354. pdr2 reveals a phosphate-sensitive checkpoint in root development. Scheres B, Benfey P, Dolan L. 2002. Root development. The Arabidopsis Plant Journal 37: 801–814. Book. American Society of Plant Biologists, doi: 10.1199/tab.0101. To JP, Haberer G, Ferreira FJ, Deruere J, Mason MG, Schaller GE, Alonso Schulze J, Temple G, Temple SJ, Beschow H, Vance CP. 2006. Nitrogen JM, Ecker JR, Kieber JJ. 2004. Type-A Arabidopsis response regulators are fixation by white lupin under phosphorus deficiency. Annals of Botany partially redundant negative regulators of cytokinin signaling. The Plant 98: 731–740. Cell 16: 658–671. Schwager KM, Calderon-Villalobos LI, Dohmann EM, Willige BC, Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J. 2006. A map Knierer S, Nill C, Schwechheimer C. 2007. Characterization of the VIER of KNAT gene expression in the Arabidopsis root. Plant Molecular Biology F-BOX PROTEINE genes from Arabidopsis reveals their importance for 60: 1–20. plant growth and development. The Plant Cell 19: 1163–1178. Trusov Y, Rookes JE, Tilbrook K, Chakravorty D, Mason MG, Serna L. 2005. Epidermal cell patterning and differentiation throughout Anderson D, Chen JG, Jones AM, Botella JR. 2007. Heterotrimeric the apical-basal axis of the seedling. Journal of Experimental Botany G protein gamma subunits provide functional selectivity in 56: 1983–1989. Gbetagamma dimer signaling in Arabidopsis. The Plant Cell 19: Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, 1235–1250. Schachtman DP. 2007. The Arabidopsis transcription factor MYB77 Ullah H, Chen JG, Temple B, Boyes DC, Alonso JM, Davis KR, Ecker JR, modulates auxin signal transduction. The Plant Cell 19: 2440–2453. Jones AM. 2003. The beta-subunit of the Arabidopsis G protein Shukla RK, Raha S, Tripathi V, Chattopadhyay D. 2006. Expression of negatively regulates auxin-induced cell division and affects multiple CAP2, an APETALA2-family transcription factor from chickpea, developmental processes. The Plant Cell 15: 393–409. enhances growth and tolerance to dehydration and salt stress in transgenic Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM. 2001. tobacco. Plant Physiology 142: 113–123. Modulation of cell proliferation by heterotrimeric G protein in Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS. Arabidopsis. Science 292: 2066–2069. 2006. Opposite root growth phenotypes of hy5 versus hy5 hyh mutants Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael correlate with increased constitutive auxin signaling. PLoS Genetics 2: G, Naudts M, Iida R, Gruissem W, Tasaka M et al. 2005. Cell cycle e202. progression in the pericycle is not sufficient for SOLITARY ROOT/ Signora L, De Smet I, Foyer CH, Zhang H. 2001. ABA plays a central role IAA14-mediated lateral root initiation in Arabidopsis thaliana. in mediating the regulatory effects of nitrate on root branching in The Plant Cell 17: 3035–3050. Arabidopsis. Plant Journal 28: 655–662. Vellosillo T, Martinez M, Lopez MA, Vicente J, Cascon T, Dolan L, Sivaguru M, Pike S, Gassmann W, Baskin TI. 2003. Aluminum rapidly Hamberg M, Castresana C. 2007. Oxylipins produced by the depolymerizes cortical microtubules and depolarizes the plasma 9-lipoxygenase pathway in Arabidopsis regulate lateral root membrane: evidence that these responses are mediated by a glutamate development and defense responses through a specific signaling receptor. Plant & Cell Physiology 44: 667–675. cascade. The Plant Cell 19: 831–846.

Verkest A, Manes CL, Vercruysse S, Maes S, Van Der Schueren E, Woodward AW, Bartel B. 2005. Auxin: regulation, action, and interaction. Beeckman T, Genschik P, Kuiper M, Inze D, De Veylder L. 2005. Annals of Botany 95: 707–735. The cyclin-dependent kinase inhibitor KRP2 controls the onset of the Woodward AW, Ratzel SE, Woodward EE, Shamoo Y, Bartel B. 2007. endoreduplication cycle during Arabidopsis leaf development through Mutation of E1-CONJUGATING ENZYME-RELATED1 decreases inhibition of mitotic CDKA;1 kinase complexes. The Plant Cell RELATED TO UBIQUITIN conjugation and alters auxin response and 17: 1723–1736. development. Plant Physiology 144: 976–987. Walch-Liu P, Liu LH, Remans T, Tester M, Forde BG. 2006. Evidence that Wu G, Lewis DR, Spalding EP. 2007. Mutations in Arabidopsis multidrug L-glutamate can act as an exogenous signal to modulate root growth and resistance-like ABC transporters separate the roles of acropetal and branching in Arabidopsis thaliana. Plant & Cell Physiology 47: 1045–1057. basipetal auxin transport in lateral root development. The Plant Cell Walch-Liu P, Neumann G, Bangerth F, Engels C. 2000. Rapid effects of 19: 1826–1837. nitrogen form on leaf morphogenesis in tobacco. Journal of Experimental Xie Q, Frugis G, Colgan D, Chua NH. 2000. Arabidopsis NAC1 transduces Botany 51: 227–237. auxin signal downstream of TIR1 to promote lateral root development. Wang H, Fowke LC, Crosby WL. 1997. A plant cyclin-dependent kinase Genes & Development 14: 3024–3036. inhibitor gene. Nature 386: 451–452. Xie Q, Guo HS, Dallman G, Fang S, Weissman AM, Chua NH. 2002. Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC. 1998. SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis auxin signals. Nature 419: 167–170. thaliana interacts with both Cdc2a and CycD3, and its expression is Xiong L, Wang RG, Mao G, Koczan JM. 2006. Identification of drought induced by abscisic acid. Plant Journal 15: 501–510. tolerance determinants by genetic analysis of root response to drought Wang X, Xu Y, Han Y, Bao S, Du J, Yuan M, Xu Z, Chong K. 2006. stress and abscisic Acid. Plant Physiology 142: 1065–1074. Overexpression of RAN1 in rice and Arabidopsis alters primordial Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P. 2005. OsPTF1, a novel meristem, mitotic progress, and sensitivity to auxin. Plant Physiology transcription factor involved in tolerance to phosphate starvation in rice. 140: 91–101. Plant Physiology 138: 2087–2096. van der Weele CM, Spollen WG, Sharp RE, Baskin TI. 2000. Growth of Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K. 2002. Arabidopsis thaliana seedlings under water deficit studied by control of Two distinct high-affinity sulfate transporters with different inducibilities water potential in nutrient-agar media. Journal of Experimental Botany mediate uptake of sulfate in Arabidopsis roots. Plant Journal 29: 465–473. 51: 1555–1562. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T. nutrient-induced changes in root architecture. Science 279: 407–409. 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple Zhang H, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for developmental alterations indicating opposite functions of cytokinins in regulation of root branching by nitrate. Proceedings of the National Academy the regulation of shoot and root meristem activity. The Plant Cell of Sciences, USA 96: 6529–6534. 15: 2532–2550. Zhang H, Rong H, Pilbeam D. 2007a. Signalling mechanisms underlying Werner T, Motyka V, Strnad M, Schmulling T. 2001. Regulation of plant the morphological responses of the root system to nitrogen in Arabidopsis growth by cytokinin. Proceedings of the National Academy of Sciences, USA thaliana. Journal of Experimental Botany 58: 2329–2338. 98: 10487–10492. Zhang J, Peng Y, Guo Z. 2007b. Constitutive expression of Williamson LC, Ribrioux SP, Fitter AH, Leyser HM. 2001. Phosphate pathogen-inducible OsWRKY31 enhances disease resistance and affects availability regulates root system architecture in Arabidopsis. Plant root growth and auxin response in transgenic rice plants. Cell Research 18: Physiology 126: 875–882. 508–521. Woll K, Borsuk LA, Stransky H, Nettleton D, Schnable PS, Hochholdinger Zolobowska L, Van Gijsegem F. 2006. Induction of lateral root structure F. 2005. Isolation, characterization, and pericycle-specific transcriptome formation on petunia roots: a novel effect of GMI1000 Ralstonia analyses of the novel maize lateral and seminal root initiation mutant solanacearum infection impaired in Hrp mutants. Molecular Plant–Microbe rum1. Plant Physiology 139: 1255–1267. Interactions 19: 597–606.

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