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A Complex Case of Simple Leaves: Indeterminate Leaves Co-Express ARP and KNOX1 Genes

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A Complex Case of Simple Leaves: Indeterminate Leaves Co-Express ARP and KNOX1 Genes Dev Genes Evol (2010) 220:25–40 DOI 10.1007/s00427-010-0326-4 ORIGINAL ARTICLE A complex case of simple leaves: indeterminate leaves co-express ARP and KNOX1 genes Kanae Nishii & Michael Möller & Catherine Kidner & Alberto Spada & Raffaella Mantegazza & Chun-Neng Wang & Toshiyuki Nagata Received: 27 November 2009 /Accepted: 15 April 2010 /Published online: 26 May 2010 # Springer-Verlag 2010 Abstract The mutually exclusive relationship between Here, we present several datasets illustrating the co- ARP and KNOX1 genes in the shoot apical meristem and expression of ARP and KNOX1 genes in the shoot apical leaf primordia in simple leaved plants such as Arabidopsis meristem, leaf primordia, and developing leaves in plants has been well characterized. Overlapping expression with simple leaves and simple primordia. Streptocarpus domains of these genes in leaf primordia have been plants produce unequal cotyledons due to the continued described for many compound leaved plants such as activity of a basal meristem and produce foliar leaves Solanum lycopersicum and Cardamine hirsuta and are termed “phyllomorphs” from the groove meristem in the regarded as a characteristic of compound leaved plants. acaulescent species Streptocarpus rexii and leaves from a shoot apical meristem in the caulescent Streptocarpus Communicated by K. Schneitz glandulosissimus. We demonstrate that the simple leaves Electronic supplementary material The online version of this article in both species possess a greatly extended basal meriste- (doi:10.1007/s00427-010-0326-4) contains supplementary material, matic activity that persists over most of the leaf’s growth. which is available to authorized users. The area of basal meristem activity coincides with the co- K. Nishii (*) : C.-N. Wang expression domain of ARP and KNOX1 genes. We suggest Institute of Ecology and Evolutionary Biology, that the co-expression of ARP and KNOX1 genes is not Department of Life Science, National Taiwan University, exclusive to compound leaved plants but is associated with Rm. 1207, Life Science Building, No.1, Sec. 4, Roosevelt Road, foci of meristematic activity in leaves. Taipei 10617 Taiwan, Republic of China e-mail: [email protected] . : Keywords ARP KNOX1 Streptocarpus Gesneriaceae M. Möller (*) C. Kidner Meristem Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK e-mail: [email protected] Introduction : A. Spada R. Mantegazza In most seed plants, the above ground parts of plants are Department of Biology, University of Milan, Via Celoria 26, formed from layered shoot apical meristems (SAMs). Milan 20133, Italy SAMs are composed of three domains that fulfill distinct functions: the central zone contains a self-renewing pool of C. Kidner stem cells, the peripheral zone from which cells are Institute of Molecular Plant Sciences, University of Edinburgh, King’s Buildings, Mayfield Road, recruited into developing organs, and the rib zone, which Edinburgh EH9 3JR, UK is the origin of ground tissue within the stem (Gifford and Corson 1971; Bowman and Eshed 2000;Carlesand T. Nagata Fletcher 2003). Leaf primordia arise from the peripheral Faculty of Bioscience and Applied Chemistry, Hosei University, 3-7-2 Kajino-cho, Koganei-shi, zone of the SAM. During leaf development, cell division Tokyo 184-8584, Japan initially occurs throughout the primordia, but soon after- 26 Dev Genes Evol (2010) 220:25–40 wards becomes limited to the base of the leaf and finally (Jong 1970; Jong and Burtt 1975). Three meristems, the cell expansion alone is responsible for the continuing “basal meristem”, “petiolode meristem”,and“groove enlargement of the leaf (Poethig and Sussex 1985a, meristem” are involved in the production of a leaf-like 1985b; Nath et al. 2003). organ termed “phyllomorph” (Fig. 1). The basal meristem The underlying genetic pathways for SAM establish- is found at the base of the lamina and is a region of ment, maintenance, and leaf development have been persistent cell division supplying new laminar tissue. The extensively studied in a number of model plants such as petiolode meristem, a diffuse rib meristematic area of the Arabidopsis, Antirrhinum, and maize. In Arabidopsis, “petiolode” (stem-like petiole of the leaf), is responsible for WUSCHEL (WUS) and CLAVATA (CLV) are key genes that petiolode and midrib extension. The groove meristem is act in the central zone, specifying the fate of the stem cells positioned on the petiolode and responsible for the and maintaining a relatively constant cell number in the formation of new organs, phyllomorphs or inflorescences SAM (Mayer et al. 1998; Fletcher et al. 1999; Schoof et al. (Fig. 1) (see also Fig. 1 in Mantegazza et al. 2007; Jong 2000). Class 1 KNOTTED-like homeobox genes (KNOX1) 1970, 1978). are also important for maintaining meristem cells in an All Streptocarpus species exhibit anisocotyly, where one undifferentiated state (Vollbrecht et al. 1991; Barton and of the two initially equal-sized cotyledons develops into a Poethig 1993; Long et al. 1996). KNOX1 genes have macrocotyledon through the extended activity of its basal undergone duplication in several different lineages, and meristem shortly after germination to form the first photosyn- studies on expression patterns and mutant phenotypes thetic organ. In acaulescent species (unifoliates and rosulates), suggest that sub- and neo-functionalizations have occurred an organized SAM is not produced between the cotyledons. (Reiser et al. 2000). In eudicots, genes of the SHOOTMER- The macrocotyledon becomes a “cotyledonary phyllomorph”, ISTEMLESS (STM)-like KNOX1 clade are required for and rosulate species initiate additional phyllomorphs from the meristem function and are expressed throughout the groove meristem while unifoliate species maintain only a meristem. Genes in the BREVIPEDICELLUS (BP)-like single enlarged cotyledon (Fig. 1) (see also Fig. 1 in Harrison clade are required for meristem function in the absence of et al. 2005a;Jong1970). The basal meristem is active until ASYMMETRIC LEAVES 1 (AS1)andSTM and are the leaves produce an inflorescence at its base, and this can expressed predominantly in the peripheral zone in Arabi- take more than 4 years in some species during which the dopsis (Byrne et al. 2000; Reiser et al. 2000). lamina continues to grow (Hilliard and Burtt 1971). ARP genes, named after the orthologous genes AS1 from Caulescent Streptocarpus species, while also showing Arabidopsis thaliana, ROUGH SHEATH2 (RS2) from anisocotyly and no embryonic SAM, quickly develop a maize and PHANTASTICA (PHAN) from Antirrhinum conventional shoot structure with stem and decussate pairs of majus, are MYB-like transcription factors involved in simple leaves from a central layered SAM produced post- adaxial–abaxial and proximal–distal axis formation during embryogenically (Jong 1970; Imaichi et al. 2007). Leaves of leaf morphogenesis. ARP genes negatively regulate KNOX1 the caulescent Streptocarpus pallidiflorus show a group of genes in determined organ primordia (Waites et al. 1998; small cells at the base, which were compared to a possible Timmermans et al. 1999; Tsiantis et al. 1999; Byrne et al. basal meristem (Imaichi et al. 2007). This may indicate that 2000). In Arabidopsis, STM represses the expression of AS1 the macrocotyledon and foliage leaf development in Strepto- in the SAM, and AS1 in turn represses BP/KNAT1 in leaf carpus share certain features. primordia (Byrne et al. 2002). This antagonistic relationship The activity of several genes, involved in meristem is characteristic of many plants with simple leaves (Waites function in model species, has previously been studied in et al. 1998; Byrne et al. 2002), but has been shown to break Streptocarpus. Immunolocalization of KNOX proteins and down in plants with compound leaves. In these, ARP and KNOX1 SSTM1 (Streptocarpus STM1) RT-PCR showed KNOX1 genes are either co-expressed in leaf primordia KNOX1 expression in the SAM and proximal region of (Cardamine hirsuta; Hay and Tsiantis 2006) or in the SAM leaves, but not in incipient leaf primordia in the SAM in the and leaf primordia (Solanum lycopersicum; Hareven et al. caulescent Streptocarpus saxorum. KNOX proteins were 1996; Chen et al. 1997; Koltai and Bird 2000). detected in inflorescences, groove meristems, and leaf Most species of the family Gesneriaceae have simple primordia of the acaulescent Streptocarpus rexii (Harrison leaves with a simple leaf primordium produced from a et al. 2005a). Further detailed studies on S. rexii revealed SAM (Lai 2001; Barth et al. 2009). Caulescent species in that SrSTM1 (S. rexii STM1) is expressed not only in the the genus Streptocarpus conform to this development. groove meristem, but also in the basal meristem of Acaulescent Streptocarpus species, though simple leaved, cotyledons (Mantegazza et al. 2007). Expression was also show a radically different organization and development of found throughout the developing embryo and in cotyledons meristems and leaves. To adequately portray the unique during early stages of germination. It was concluded that features in these species, special terms were introduced KNOX1 gene expression is tightly linked to meristematic Dev Genes Evol (2010) 220:25–40 27 Fig. 1 The unique growth patterns in Streptocarpus. a–d The rosulate Streptocarpus species. e 4–7 Acaulescent (rosulate, unifoliate) species. Streptocarpus rexii. a 1 Isocotylous stage 15 DAS. a 2 Anisocotylous e 4 The macrocotyledon develops into the “cotyledonary phyllo- stage 30 DAS. a 3 Anisocotylous seedling with first phyllomorph 65 morph” and forms a groove meristem on the petiolode. e 5 In rosulate DAS. a 4 Seedling with several leaves 90 DAS. Bars, 1 mm. b–d species, the first true leaf, or “primary phyllomorph” is formed from SEM images. b Top view and c side view of anisocotylous seedling. d the groove meristem of the macrocotyledon. e 6 Front view of a single Magnified view of c, showing the basal meristem and groove phyllomorph. e 7 TS off-center as indicated (dashed line) through a meristem. e Schematic illustration of seedling development in phyllomorph. ab abaxial (lower), ad adaxial (upper) leaf surface, b Streptocarpus (modified from Jong 1970; Jong and Burtt 1975).
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