Available online at www.sciencedirect.com ScienceDirect

Rice Science, 2020, 27(6): 468−479

Review

Development of Rice : How Histocytes Modulate Polarity Establishment

# # WANG Jiajia , XU Jing , QIAN Qian, ZHANG Guangheng (State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou 310006, China; #These authors contributed equally to this work)

Abstract: An ideal leaf shape is beneficial to the yield of rice. Molecular understanding of the leaf primordia and polarity establishment plays a significant role in exploring the genetic regulatory network of leaf morphogenesis. In recent years, researchers have cloned an array of coding genes and a few non-coding small RNAs involved in rice leaf development through regulating the development of leaf primordia, vascular bundles, sclerenchyma cells, bulliform cells, cell walls and cells. These genes and their interactions play critical roles in rice leaf development through the determination and regulatory role in gene expression, and their coordination with other genetic networks or signal pathways. But the relationship among these genes is poorly defined and the underlying network is still unclear. In this review, we introduced the regulatory pathways of leaf primordium development and leaf polarity establishment, mainly the relationship between cell development mechanism and leaf polarity establishment, focusing on how leaf affects leaf shape. Hopefully, the regulation network reviewed here has immediate implications for future research and genomic design breeding. Key words: rice; leaf morphogenesis; molecular mechanism; tissue cell; leaf polarity establishment

Leaf is the determinate organ that serves as a main The normal development of leaf tissue is essencial photosynthetic structure of plants (Piazza et al, 2005). to the maintenance of leaf morphology, which differs Leaf architecture is closely related to environmental across species (Hasson et al, 2010). Rice leaves have factors such as light intensity, temperature and humidity, the typical characteristics of monocotyledonous leaves which influences plant transpiration, stress resistance, with no palisade tissues or sponge tissues in mesophyll photosynthetic efficiency and other physiological cells and no known difference in the distribution of characteristics (Mishra and Panda, 2017; Liu et al, stomata between the upper and lower epidermis. The 2018; Zhang et al, 2018; Chen T et al, 2019). Lamina normal developments of vascular bundles, bulliform posture is an important agronomic trait closely associated cells, sclerenchyma cells, epidermal cells, stomata and with plant type. The regulation of leaf posture is cell walls form the premise for the maintenance of the considered as an effective means to improve crop yield. isobilateral leaf of rice. In recent years, many genes or Leaf development includes primordium initiation, quantitative trait locus (QTLs) related to leaf morpho- tissue differentiation, polarity establishment, leaf extension genesis have been cloned. They are involved in the and maturation. Adaxial-abaxial leaf polarity, proximal- signaling pathways of phytohormone, transcription distal leaf polarity, and median-lateral leaf polarity factors, microRNAs, and regulates leaf shape through form a three-dimensional axial polarity that directly the division and differentiation of cells in leaf. determines leaf morphology (Itoh et al, 2008). Furthermore, the abnormal developments of vascular

Received: 25 December 2019; Accepted: 9 May 2020 Corresponding authors: ZHANG Guangheng ([email protected]); QIAN Qian ([email protected]) Copyright © 2020, China National Rice Research Institute. Hosting by Elsevier B V This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) Peer review under responsibility of China National Rice Research Institute http://dx.doi.org/10.1016/j.rsci.2020.09.004

(C skelaton, Osmotic regulation, N storage, Insect Deterrant) 2

. WANG Jiajia, et al. How Histiocytes Modulate Leaf Polarity Establishment 469 bundles, sclerenchyma cells, bulliform cells, epidermis cells (Ito et al, 2001). Furthermore, studies have and cell walls also lead to the alterment of leaf shown that the expression of KNOX is positively architecture (Fig. 1). This paper provided an overview regulated by cytokinin and KNOX itself. The positive of the relationship between cell development and leaf self-regulation of OSH1 is essential for the shape, with an emphasis on leaf polarity and leaf maintenance of the rice apical (Tsuda et al, primordium development, which may contribute to the 2011). Further studies have shown that OSH1 inhibits understanding of leaf morphogenesis mechanism at the brassinosteroid (BR) pathway by activating its cellular level, and provide foundation for the further catabolic gene, thereby controlling the establishment elucidation of leaf morphogenesis mechanisms. and maintenance of SAM (Tsuda et al, 2014). Another member of the rice KNOX family class I gene, Leaf primordium development affects OSH71/Oskn2, interacts with the growth regulator rice leaf polarity establishment OsGRF3, which acts as a transcriptional repressor involved in the regulation of Oskn2-mediated SAM Shoot apical meristem (SAM) is at the top of the stem formation (Postma-Haarsma et al, 1999; Kuijt et al, and forms the birthplace of both leaves and stems. The 2014). Long-chain fatty acid ω-alcohol dehydrogenase initiation and maintenance of SAM are required for ONI3 inhibits the expression of KNOX (Akiba et al, the continuous development of the stem (Hasson et al, 2014), which in turn inhibits the accumulation of 2010). As a major phytohormone, auxin precisely auxin and regulates the growth and development of regulates the primordium differentiation of SAM rice shoots (Fang et al, 2015). The mutual antagonism (Guenot et al, 2012), and induces differentiation of of KNOX I and the MYB family ASYMETRIC organ primordium during the early stages of leaf LEAVES1/ROUGH SHEATH2/PHANTASTICA (ARP) development (Kalve et al, 2014). High concentrations proteins in Arabidopsis are key to the initiation of leaf of auxin inhibit the activity of KNOTTED-like primordia. ARP inhibits the activity of KNOX at the homebox 1 (KNOX1) (Su et al, 2011), which positively primordium, whilst KNOX is highly expressed in all regulates the biosynthesis of cytokinin and negatively meristematic tissues outside the primordial start site regulates the synthesis of gibberellin (GA) through (Byrne et al, 2000, 2002). inhibiting the activity of GA20ox (Kalve et al, 2014). Normal initiation of the leaf is essential to morphogenesis of late leaves. Phyllotaxy and Members of the KNOX gene family have important plastochron form the basis of plant architecture regulatory roles in the initiation of leaf primordia and the (Miyoshi et al, 2004). The plastochron genes PLA1 correct establishment of the leaf apical axis (Hay and and PLA2 mediate leaf maturation and the temporal Tsiantis, 2009). Rice KNOX family class I gene OSH1 pattern of successive leaf initiation (Mimura and Itoh, is expressed prior to organ differentiation in specific 2014). PLA1 encodes cytochrome P450 CYP78A11, regions during early embryogenesis (Sato et al, 1996). and affects initial development of leaves and The class I homeodomain gene of the KNOX family termination of vegetative growth (Miyoshi et al, 2004). plays an important role in the formation and PLA2/LHD2 encodes an RNA-binding protein that maintenance of the undetermined meristematic state of regulates rice shoot development through KNOX and hormone-related genes (Xiong et al, 2006). PLA1 and PLA2 play a key role in the downstream of gibberellin (GA) signaling pathway and regulate leaf maturation (Mimura et al, 2012). PLA3/GO encodes a glutamate carboxypeptidase II, which is expressed in the whole plant body and can catabolize small peptides, regulating various signaling pathways involved in a number of processes. The loss-of-function mutant of PLA3 shows similar phenotypes to pla1 and pla2. Furthermore, pla3 shows pleiotropic phenotypes, including enlarged embryo, seed vivipary, defects in Fig. 1. Overview of tranverse section of rice leaf. BC, Bulliform cell; LV, Large vascular bundle; SV, Small vascular SAM maintenance and abnormal leaf morphology bundle; SC(ad), Sclerenchyma cell (adaxial); SC(ab), Sclerenchyma (Kawakatsu et al, 2009). Though the regulatory cell (abaxial). mechanism of early initiation of leaf primordia has

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Adaxial domain Abaxial domain A Initiation of leaf Establishment and B primordia maintenance of SAM miR165/166 AGO1

ZPR CK BR signal pathway

ONI3 KANADI IPT7 AUX1 HD-ZIP III

ARP KNOX1 Auxin maximum PIN1 ARP (AS1/AS2) YABBY WOX3

GA 2ox GA20-ox GRF3

GA3ox2 Maintain the meristem in an tasiRNA ARF3/4 GA undifferentiated state

Fig. 2. Genetic and molecular network controlling initiation of leaf primordia (A) and adaxial-abaxial leaf polarity (B). ↑ indicates acceleration; indicates inhibition. been clearly defined (Fig. 2-A), the regulatory role of class III gene, OSHB4, regulates leaf development in different tissue structures in the establishment of leaf an auxin-dependent manner in rice (Li Y Y et al, 2016). polarity is not well understood. miRNA165/166 regulates the adaxial-abaxial polarity of leaves by inhibiting the HD-ZIP class III gene Tissue structure regulates rice leaf polarity (Zhang et al, 2018). Moreover, OsAGO1b negatively development regulates the accumulation of miRNA166 and trans- Among the three axial polarities of the blade, the acting small interfering RNAs (ta-siRNAs) (Li et al, adaxial-abaxial polarity has the greatest influence on 2019). The YABBY gene and WOX gene are essential blade morphogenesis. In the regulatory mechanisms of for plant lateral organ formation and meristem the adaxial-abaxial polarity in Arabidopsis thaliana, function. A WUSCHEL-like homologous gene, WOX3, maize and snapdragon, multiple transcription factors inhibits the expression of YAB3, which is required for and microRNAs (miRNAs) participate in the regulatory rice leaf development (Dai et al, 2007a). OsYABBY1 network of leaf primordium development, as well as binds to a GA response element in the GA3ox2 the maintenance or establishment of leaf morphology. promoter and is involved in the feedback regulation of The regulatory network of leaf adaxial-abaxial polarity rice GA synthesis (Dai et al, 2007b). in these model plants has been elaborated (Fig. 2-B), in Leaf length, width and the curling degree of mature which class III HOMEODOMAIN-LEUCINE ZIPPER rice leaves are the final evaluation indexes of the three- (HD-ZIP III) and AS1/AS2 complexes promote adaxial dimensional body axis of leaf polarity development, characteristics, and KANADIs, YABBY and ARF3/ARF4 and these indexes also determine the effective promote abaxial characteristics (Hasson et al, 2010). photosynthetic area and photosynthetic efficiency of Furthermore, the SHAQKYF-like MYB transcription plants. An abnormal morphology and altered number factor SHALLOT-LIKE 1 (SLL1) in rice, which belongs of single or multiple tissues and cells, such as the to the KANAD I-like transcription factor family, abaxial surface sclerenchyma cells, bulliform cells, participates in the regulation of leaf abaxial polarity vascular bundles, epidermis, cell walls and cuticles, through regulating programmed cell death of abaxial lead to changes in leaf size and polarity development. mesophyll cells of the leaves (Zhang et al, 2009). The Cell division or elongation affects leaf tissue rice YABBY gene family member OsYABBY1 is development specifically expressed in the putative precursor cells of both the mestome sheath in the large vascular Abnormal cell division or elongation leads to changes bundle and the abaxial sclerenchyma in the leaves, in plant organ. The growth-regulating factor (GRF)- where it participates in the regulation of the leaf interacting factor gene OsGIF1 (He et al, 2017), abaxial surface polarity (Toriba et al, 2007). A HD-ZIP K+/Na+/Cl‒ cotransporter OsCCC1 (Chen et al, 2016)

WANG Jiajia, et al. How Histiocytes Modulate Leaf Polarity Establishment 471 and NAL8 (Chen K et al, 2019) positively regulate cell The synthesis and polar transport of auxin also have elongation, which results in the changes of cell size important functions in the regulation of vascular and leaf size. The loss-of-function of these genes leads bundle development, which in turn affect leaf morphology. to the formation of narrow leaves, and an altered 3D TRYPTOPHAN DEFICIENT DWARF 1 (TDD1) (Sazuka polarization axis. The loss-of-function of OsGIF1 not et al, 2009), NARROW ALBINO LEAF 1 (OsNAAL1) only inhibits cell elongation, but also affects the (Xu J et al, 2017) and NARROW LEAF 7 (NAL7) / number and morphology of bulliform cells (He et al, CONSTITUTIVELY WILTED1 (OsCOW1) (Woo et al, 2017). Small auxin-up RNA OsSAUR4 negatively 2007; Fujino et al, 2008) regulate leaf vascular bundle regulates cell elongation and affects leaf morphology development and influence leaf morphogenesis through through its inhibition of auxin synthesis and transport participating in the tryptophan-dependent indole acetic (Xu Y X et al, 2017). DWARF and GLADIUS LEAF 1 acid (IAA) biosynthetic pathway. The rice narrow-leaf (DGL1) also negatively regulates cell elongation. A gene NAL1 encodes a serine/cysteine protease that loss-of-function mutation of DGL1 results in disordered plays an important role in the lateral growth of leaves. microtubules in cortical cells, abnormal longitudinal The loss-of-function of NAL1 significantly reduces the cell elongation, and formation of large and distorted polar transport of auxin, affecting the number and cells (Komorisono et al, 2005). Dwarf gene D1 arrangement of leaf vascular bundles (Zhang et al, positively regulates cell division, and its regulation of 2014; Jiang et al, 2015; Lin et al, 2019). The RICE plant morphology is mainly achieved through its MINUTE-LIKE 1 gene (RML1) encodes the ribosomal participation in GA signaling via the Gα protein large subunit protein L3B, the main function of which (Fujisawa et al, 1999). Rice STEMLESS DWARF 1 is to regulate ribosome synthesis and auxin distribution (STD1), which encodes a homolog of the A. thaliana or transport. The loss-of-function of RML1 causes a PAKRP2, inhibits cell division and organ development loss of auxin polar transport and a reduction in large through reducing the ATPase activity of its coding and small vascular bundles, leading to reduced leaf protein (Fang et al, 2018). widths (Zheng et al, 2016). The development of vascular bundles in rice leaves Vascular system influences leaf morphology is additionally influenced by the alternative splicing of The plant vascular system consists of and mRNA and the cutting of miRNA. The GATA zinc , which are specialized for the transportation of finger domain protein SNFL1 affects the size of rice water and photoassimilates, respectively. The curling flag leaves through alternative splicing of mRNA, leaf phenotype is directly related to the water transport with decreasing lengths of epidermal cells and reducing in the xylem (Zhang et al, 2018). The number of large numbers of vascular bundles in the flag leaves of the and small vascular bundles directly affects the blade mutant plant, which is the major mechanism governing width. The development of the vascular system is decreased leaf width (He et al, 2018). Osa-miR319b regulated by genetic and plant endogenous hormones. positively regulates vascular bundle development and For example, as a member of the WUSCHEL- influences leaf width through its activity on target RELATED HOMEOBOX gene family, OsWOX4 genes including OsPCF6 and OsTCP21 (Wang et al, positively regulates the maintenance of , 2014). with OsWOX4 downregulation leading to decreased Bulliform cells decide the fate of leaf adaxial surface endogenous cytokinin synthesis, an arrest of vascular bundle differentiation, a defect in midrib formation Bulliform cells are large, thin-walled and highly and cell maintenace, as well as narrowing vacuolated cells which exist in groups between the of leaf width (Yasui et al, 2018). OsWOX3A is vasculatures in leaf adaxial surface. Changes in the involved in the negative feedback regulation of GA number, size or distribution of bulliform cells lead to response and GA synthesis, positively regulating leaf alteration in leaf rolling index. The appearances of horizontal axis growth and vascular bundle formation rolled leaf phenotype in many identified mutants with (Cho et al, 2016). As a member of the plant OVALE rolled leaves are due to the defective development of family, OsOFP2 regulates GA biosynthesis, the the bulliform cells in adaxial side (Zhou et al, 2018), inhibition of which limits the vascular bundle including oul1 (Zou et al, 2011), rel1 (Chen et al, development of leaves, leading to changes in leaf 2015), sll2 (Zhang J J et al, 2015) and hal1 morphology (Schmitz et al, 2015). (Matsumoto et al, 2018). REL1 (Chen et al, 2015) and

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REL2 (Yang et al, 2016) affect leaf curling by directly abaxial side, thereby resulting in incurved leaves or indirectly regulating the size and number of (Zhang et al, 2009). Similarly, SEMI-ROLLED LEAF bulliform cells. ABAXIALLY CURLED LEAFS (ACLs) 2 (SRL2), NARROW AND ROLLED LEAF 2 (NRL2) play an important role in development of bulliform and ABNORMAL VASCULAR BUNDLES (AVB) are cells. Overexpressions of ACL1 and ACL2 increase allele genes that regulate leaf architecture through bulliform cells and induce abaxial curling of leaf encoding plant-specific proteins. Mutation of SRL2 blades in rice (Li et al, 2010). Rice outermost cell- leads to the reduction of the abaxial sclerenchyma specific gene 5 (Roc5), a member of the HD-ZIP class cells in the leaf and thus results in curled leaf; at the IV family, negatively regulates the fate and development same time, the altered numbers of cells and bundles of bulliform cells. The increasing numbers and sizes lead to reduced leaf width (Liu et al, 2016; Zhao et al, of the bulliform cells in the leaf adaxial side of 2016; Ma et al, 2017). OsYABBY1 in rice is closely Roc5-overexpressing lines and PROTODERMAL related to the differentiation of sclerenchyma cells, FACTOR LIKE (PFL)-RNAi transgenic plants lead to which in turn affects leaf morphology (Toriba et al, reverse rolling leaves (Zou et al, 2011). In over- 2007). MiR166-OsHB4 regulates the expression of expressing lines of OSHB4, a HD-ZIP class III gene, downstream genes related to polysaccharide synthesis, the bulliform cells at the adaxial side are reduced, and and affects the development of sclerenchyma cells. leaves are curled to the adaxial side (Li Y Y et al, Leaves of miRNA166 knockout lines are adaxiallly 2016). Similarly, LEAF ROLLING RECEPTOR-LIKE rolled with abnormal sclerenchyma cells (Zhang et al, CYTOPLASMIC KINASE 1 (LRRK1) affects leaf 2018). ADAXIALIZED LEAF 1 (ADL1) encodes a rolling by negatively regulating the development of cysteine protease that is orthologous to maize bulliform cells. The sizes of bulliform cells in LRRK1 DEFECTIVE KERNEL1. Mutations in ADL1 result in overexpressing lines are reduced, resulting in leaf adaxialization as the leaves are covered with adaxially rolling leaves (Zhou et al, 2018). The bulliform-like cells that are excusively distributed on LATERAL ORGAN BOUNDARIES DOMAIN (LBD) the adaxial surface, leading to abaxially rolled leaves gene OsLBD3-7 acts as an upstream regulatory gene (Hibara et al, 2009). Argonaute (AGO) protein is a for the development of bulliform cells, and the major member of the RNA-induced silencing complex overexpression of it leads to decrease of the numbers (RISC) complex, and AGO1 regulates growth and and sizes of the bulliform cells, resulting in leaf development of plants through recruiting small RNAs narrowing and curling to the adaxial side (Li C et al, regulating the expression of related genes. OsAGO1b, 2016). Changes in the morphology of the bulliform one of the AGO genes in rice, regulates leaf morphology cells also lead to changes in leaf morphology. by affecting the differentiation of abaxially sclerenchyma NAL7/OsCOW1, a member of the rice YUCCA gene (a cells during rice leaf development. The overexpression flavin monooxygenase-like enzyme gene) family, of OsAGO1b results in a decrease in the accumulation participates in the biosynthesis of IAA and affects the of miRNA166 and ta-siRNA, which in turn induces ratio of root/shoot, leading to changes in the water the corresponding target genes OsHBs and OsARFs to balance of plants. Morphological changes of the be significantly up-regulated in the region where bulliform cells caused by the dehydration of oscow1 vascular bundles and sclerenchyma cells are leaves result in narrowing and adaxial curled leaves differentiated. These lead to the disappearance of leaf (Woo et al, 2007; Fujino et al, 2008). abaxial sclerenchyma cells and subsequently curled blades (Li et al, 2019). Sclerenchyma cells and leaf abaxial surface morphogenesis Effects of cell wall on rice leaf morphology In addition to vascular bundles, sclerenchyma cells The development of cell walls not only limits cell size, also play an important role in the maintenance of the but also mediates water transport in leaves, ultimately flat morphology of isoplanar leaves in rice. The affecting leaf morphology. The cell wall loosening development of sclerenchyma cells is closely related protein OsEXPB2 (β-expansin) positively regulates to changes in leaf curling. The deficiency of SLL1, cell size through cell wall loosening, which in turn whose main function is to determine the development affects plant morphology (Zou et al, 2015). Microtubule of the abaxial sclerenchyma cells of the leaf, leads to a depolymerase OsKinesin-13A regulates cell size defect in the formation of sclerenchyma cells on the through the orientation of cellulose microfibers in cell

WANG Jiajia, et al. How Histiocytes Modulate Leaf Polarity Establishment 473 walls (Deng et al, 2015). ROLLING-LEAF 14 (RL14) positively regulates the elongation of mesophyll cells, regulates the components of the secondary cell walls, thus affecting the development of the leaf proximal- resulting in the loss of water in leaves, abnormal distal polarity. The loss-of-function mutants of OsKS2 morphology of the bulliform cells and rolled leaves have closely arranged mesophyll cells and shorter (Fang et al, 2012). miRNA166 affects cell wall blades (Ji et al, 2014). Abnormalities in stomatal formation through its target gene OsHB4, which development affect water balance and leaf morphology. regulates downstream genes involved in polysaccharide LS1 encodes a ribonuclease H2 large subunit A synthesis (Zhang et al, 2018). DWARF and NARROWED (RNaseH2A) that mediates repair of DNA damage. LEAF 1 (DNL1) / NARROW and ROLLED LEAF 1 Under high temperatures and high light stress, the (NRL1) encodes a cellulose synthase-like protein D4, stomata in the white region of the leaves of ls1 mutants which belongs to the glycosyltransferase family. lead to extremely poor water retention and shrinking Furthermore, it affects the development of leaf of both bulliform cells and epidermal parenchyma longitudinal veins and adaxial bulliform cells through cells. The white regions of the mutant leaves are regulation of cell wall synthesis (Hu et al, 2010; Ding slightly involute and atrophied (Qiu et al, 2019). et al, 2015). The R2R3 MYB transcription factor MYB103L, which is homologous to Arabidopsis Perspective AtMYB103, regulates leaf morphology through participating in GA-mediated cellulose synthesis and Leaf morphogenesis involves the development of secondary wall formation (Yang et al, 2014; Ye et al, various tissues and multiple cell types, of which 2015). OsSND2, a member of the NAC transcription complex molecular mechanisms highly depend on the factor family, binds to the OsMYB61 promoter region systematic analysis of the genetic network. To date, and positively regulates the biosynthesis of secondary through screening various rice mutants of leaf shape in cell walls. The rolled leaf phenotype in OsSND2 double haploid or recombinant inbred line populations, overexpressing lines is due to the enhanced cell wall more than 60 genes/QTLs have been isolated (Table 1). thickness of the sclerenchyma cells (Ye et al, 2018). Although studies on the regulatory mechanisms of Effects of other tissue cells on rice leaf morphogenesis individual leaf tissue have initially performed, our knowledge of the synergistic development of different Epidermal cells and cuticle of plant leaves are often tissues and the interaction mechanism of genes associated with transpiration and are the major medium responsible for leaf morphogenesis at cellular level of environment acting on leaves. SEMI-ROLLED remain limited. In other words, the isolated genes LEAF1 (SRL1) / CURLED LEAF and DWARF 1 (CLD1) related to leaf polarity establishment fail to provide influences leaf morphology through the regulation of sufficient genetic regulatory information on rice leaf epidermal cell development and the formation of morphogenesis. In future, using multi-genetic population secondary cell walls. The appearance of bulliform-like joint analysis and genome wide association study cells in the epidermal layer (adaxial and abaxial (GWAS) technology, new genes related to leaf surface) of cld1 destroys the integrity of epidermal morphogenesis can be effectively identified. On this cells, resulting in the loss of water-holding capacity of foundation, regulatory relationship among these genes leaves (Xiang et al, 2012; Li et al, 2017). CURLY and the related signaling pathways can be further FLAG LEAF 1 (CFL1) negatively regulates the explored and the genetic regulatory network of leaf development of leaf cuticles through controlling the morphogenesis can be perfected, laying a theoretical function of HDG1 and its downstream genes BDG and foundation for the development of rice molecular FDH, leading to changes in leaf morphology (Wu et al, improvement in leaf shape. In order to make readers 2011). The rice OsCHR4 gene, which encodes a CHD3 better understand our review, we built a hypothetical chromatin remodeling factor, negatively regulates model for showing roles of the related gene in epithelial waxy synthesis and the establishment of leaf regulating leaf morphology at the cellular level (Fig. adaxial-abaxial and median-lateral polarity. Mutation 3). According to the model, under the roles of different of OsCHR4 leads to narrower and rolled leaves with genes involved in cell elongation or division, as well increased cuticular wax and decreased bundles (Guo as vascular bundle, sclerenchyma cell, epidermal cell, et al, 2019). Kasqualene synthase OsKS2, which stoma and cell wall development, rice plants exhibit mainly involves in the early biosynthesis of GA, the final phenotype of leaf lamina. Following the early

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Table 1. Lists of genes controlling rice leaf morphology.

Gene symbol Gene function Effect on leaf tissue Reference NAL1/LSCHL4 Trypsin-like serine/cysteine protease Cell division, cell expansion and vascular Zhang et al, 2014; Jiang et al, development 2015; Lin et al, 2019 OsWOX4 WUSCHEL-RELATED HOMEOBOX gene family Cell division and vascular differentiation Ohmori et al, 2013; Yasui et al, 2018 SNFL1/NL1 GATA family Cell expansion and vascular development He et al, 2018 TDD1/OASB1 Rice anthranilate synthase β-subunit Cell expansion and vascular development Sazuka et al, 2009 NRL1/OsCSLD4 Cellulose synthase-like d4 Cell expansion and vascular development Hu et al, 2010 LPA1/OsIDD14 INDETERMINATE DOMAIN protein Cell division and cell expansion Wu et al, 2013 OsJar1/OsGH3-5 Jasmonic acid-amino acid synthetase Cell division Zhang S N et al, 2015 SG1 Unknown Cell division Nakagawa et al, 2012 OsARF18/OsARF10 Auxin response factor Cell division Huang et al, 2016 SGL1 SG1-like protein 1 Cell division Nakagawa et al, 2012 D1/RGA1 GTP-binding α-subunit of heterotrimeric G protein Cell division Izawa et al, 2010 STD1 A phragmoplast-associated kinesin-related protein Cell division Fang et al, 2018 OsSAUR45 Small auxin-up RNA Cell expansion Xu Y X et al, 2017 OsVPE3 Vacuolar processing enzyme/cysteine proteinases Cell expansion Lu et al, 2016 RPL3B/RML1 Ribosome large subunit protein 3b Cell expansion Zheng et al, 2016 OsCCC1 Cation-chloride cotransporter Cell expansion Chen et al, 2016 GL7/GW7/OsFLW7 LONGIFOLIA protein Cell expansion Wang et al, 2015 GL7NR Negative regulator of GL7 Cell expansion Wang et al, 2015 DGL1 Microtubule-severing katanin-like protein Cell expansion Komorisono et al, 2005 OsARF19/OsARF7a Auxin response factor Cell expansion Zhang S N et al, 2015 OsOFP2 Ovate family protein 2 Cell expansion Schmitz et al, 2015 OsGIF1 GRF-interacting factor 1, putative, expressed Cell expansion He et al, 2017 OsNAAL1/CHR729 Chromodomain helicase/ATPase DNA-binding protein Vascular development Xu J et al, 2017 Osa-miR319a MicroRNA319 Vascular development Yang et al, 2013 Osa-miR319b MicroRNA319 Vascular development Yang et al, 2013 NAL9/VYL/ClpP Plastidic caseinolytic protease Vascular development Li et al, 2013 OsIAA3 Rice auxin/indole acetic acid gene Vascular development Nakamura et al, 2006 OsWOX3A WUSCHEL-related homeobox 3A Vascular development Ishiwata et al, 2013; Ohmori et al, 2013; Cho et al, 2016 OsARVL4 Insoluble protein, putative, expressed Vascular development Wang et al, 2016 REL2 Unknown function protein containing DUF630 and Bulliform cell development Yang et al, 2016 DUF632 domains REL1 Unknown Bulliform cell development Chen et al, 2015 ACL1 With unknown conserved functional domains Bulliform cell development Li et al, 2010 OsZHD1/ACL-D Zn-finger transcription factor Bulliform cell development Xu et al, 2014 Roc5/oul1 Homeodomain leucine zipper class IV gene Bulliform cell development Zou et al, 2011 LRRK1 Receptor like cytoplasmic kinases (RLCKs) Bulliform cell development Zhou et al, 2018 OsLBD3-7 Lateral organ boundaries domain gene Bulliform cell development Li C et al, 2016 OSHB4/OsHox32 Class III homeodomain Leu zipper (HD-ZIP class III) Bulliform cell development Li Y Y et al, 2016 OsYABBY6 YABBY gene Bulliform cell development Xia et al, 2017 OsCOW1/NAL7 Flavin-containing monooxygenase Bulliform cell and vascular development Fujino et al, 2008 ADL1/OsDEK1 Plant-specific calpain-like cysteine proteinase Sclerenchyma cell development Hibara et al, 2009 OsAGO1b AGO gene Sclerenchyma cell development Li et al, 2019 SLL1 SHAQKYF class MYB family transcription factor Sclerenchyma cell development Zhang et al, 2009 OsYAB1/OsYABBY1 YABBY gene Sclerenchyma cell development Dai et al, 2007b SRL2/AVB/NRL2 A protein with unknown function Sclerenchyma cell development Liu et al, 2016; Zhao et al, 2016; Ma et al, 2017 OsMYB103L/CEF1 R2R3-MYB transcription factor Cell wall development Yang et al, 2014 SRS3/OsKinesin-13A Microtubule depolymerase Cell wall development Deng et al, 2015 OsEXPB2 β-expansin gene Cell wall relaxation Zou et al, 2015 OsSND2 No apical meristem protein, putative, expressed Thickness of sclerenchyma cell wall Ye et al, 2018 RL14 2OG-Fe (II) oxygenase family protein Secondary cell wall formation Fang et al, 2012 CLD1/SRL1 Glycosylphosphatidylinositol-anchored protein Epidermal cell development Xiang et al, 2012 OsKS2/OsKSL2 Ent-beyerene synthase Mesophyll cell development Ji et al, 2014 ONI3/Mini1 Long-chain fatty acid ω-alcohol dehydrogenase Leaf primordium development Fang et al, 2015 WSL1 β-ketoacyl CoA synthase Leaf wax biosynthesis Yu et al, 2008 CFL1 WW domain protein Cuticle development Wu et al, 2011 OsCHR4 CHD3 family chromatin remodeler Cuticular wax biosynthesis Guo et al, 2019

WANG Jiajia, et al. How Histiocytes Modulate Leaf Polarity Establishment 475

Leaf morphology

Leaf primordium development Leaf polarity establishment

Proximal-distal leaf polarity or Adaxial-abaxial leaf polarity median-lateral leaf polarity Tissue structure

Cell division or elongation Vascular system Bulliform cell Sclerenchyma cell

STD1, OsGIF1, OsCCC1, OsWOX4, OsWOX3A, ACL1, REL1, SLL2, REL2, SLL1, SRL2, OsYABBY1, NAL8, OsSAUR4, DGL1, OsOFP2, TDD1, NAL7, Roc5, miRNA166-OsHB4, miR166-OsHB4, ADL1, D1, STD1 OsNAAL1, RML1, SNFL1 LRRK1, OsLBD3-7 OsAGO1b

Cell size or morphology

Cell wall Other tissues

OsEXPB2, OsKinesin-13A, RL14, miRNA166- SRL1, CFL1, OsCHR4, OsHB4, DNL1, MYB103L, OsSND2 OsKS2, LS1

Fig. 3. Hypothetical model for roles of genes in regulating leaf morphology. initiation of leaf primordia, leaf establishes its basic regulatory roles of genes in different tissues of rice architecture with a 3D polarization axes. The normal leaf, and combine bioinformatics and gene manipulation development of sclerenchyma cells and bulliform cells techniques to serve rice molecular design breeding. To affects the establishment and maintenance of adaxial- date, China has made breakthroughs in rice multi-gene abaxial leaf polarity. Proximal-distal leaf polarity or pyramiding and gene editing. However, further studies median-lateral leaf polarity are partially affected by are urgently required to strengthen our knowledge of cell number, cell size and vein number in leaf. regulatory mechanism of important traits by identifying Furthermore, impaired stomata, defective development more functional genes that are related to important of cell wall, incomplete epidermal cells, reduced water agronomic traits. retaining capacity and disordered mesophyll cells are The innovation and development of rice breeding in also main cause of abnormal leaf size or leaf rolling. China have significant influences on future food Molecular improvement in leaf shape plays a security. The identification of new genes responsible significant role in rice high-yielding breeding with for leaf morphogenesis and the effective application of ideal plant type. Although the photosynthesis efficiency them in breeding progress contribute to the combination in some rice mutants of moderate leaf shape is of theory and practice. It is beneficial for the relatively high, these mutants are typically accompanied establishment and improvement of molecular design by multiple agronomic traits which are not conducive technology system for ideal plant type breeding in rice. to high yields. Given this, not all high photosynthetic These will promote the transition from traditional efficiency plants are suitable for direct application in breeding to precision breeding, with greatly improvement rice breeding and production. In recent years, in the efficiency and technology of rice breeding. breakthroughs in genome editing technology have improved the efficiency of molecular design of target genes whilst avoiding alterations in the overall stability ACKNOWLEDGEMENTS of the target genome. The higher targeting efficiency has broadened its application prospect, narrowing This work was supported by grants from the National breeding population and shortening breeding cycle. In Natural Science Foundation of China (Grant Nos. future studies, we will explore the developmental 31861143006, 31901483 and 31770195), National

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