Data_Sheet_3_All together now: Cellular and molecular aspects of leaf development in lycophytes, ferns, and seed plants.FASTA

Recent advances in plant developmental genetics together with rapid accumulation of transcriptomic data on plants from divergent lineages provide an exciting opportunity to explore the evolution of plant morphology. To understand leaf origin in sporophytes of land plants, we have combined the available molecular and structural data on development of leaves with different morphologies in different plant lineages: clubmosses, spikemosses, leptosporangiate ferns, ophioglossioid ferns, marattioid ferns, whisk ferns, horsetails, and conifers. Specifically, we address the peculiarities of proximo-distal, ad/abaxial, and lateral development; presence/absence of mesophyll differentiation into palisade and spongy parenchyma; and type of leaf vascular bundles (collateral and bicollateral). Furthermore, taxon-specific and morphology-specific features of leaf development are considered in the context of the organization of shoot apical meristems (SAMs)—monoplex, simplex, or duplex—that produce leaf primordia. The data available imply that cellular patterns of leaf initiation correlate strongly with the structure of the SAMs but not with further leaf development or morphology. The later stages of leaf development are neither correlated with SAM structure nor with taxonomy. Occurrence and, if available, patterns of expression of homologs of the angiosperm genes responsible for the development of adaxial (ARP and C3HDZ) and abaxial (YABBY and KANADI) leaf domains, or establishment of the leaf marginal meristem (WOX) are discussed. We show that there is no correlation in the set of homologs of TFs that regulate abaxial and adaxial leaf domain development between leaves containing only spongy and no palisade mesophyll (of spikemosses, clubmosses, whisk ferns, horsetails, and most conifers), and leaves differentiated into palisade and spongy mesophyll (of leptosporangiate ferns, Ginkgo, Gnetum, and angiosperms). Expression of three out of four regulators of leaf development in primordia of both leaves and sporangia—C3HDZ in spikemosses and whisk ferns, YABBY in clubmosses and KANADI in spikemosses and horsetails—indicates that a sporangium developmental program could have been co-opted as a “precursor program” for the origin of microphylls and euphylls. Additionally, expression of leaf development regulators in SAMs of spikemosses (ARP, C3HDZ, and KANADI), clubmosses (YABBY), leptosporangiate ferns (C3HDZ), and horsetails (C3HDZ and KANADI) indicates that at least some mechanisms of SAM regulation were co-opted as well in the pre-program of leaf precursors.

近年来，植物发育遗传学的重要进展，加之来自不同演化支系的植物转录组数据（transcriptomic data）快速积累，为探索植物形态演化提供了极具潜力的研究契机。为解析陆生植物孢子体（sporophytes）的叶片起源问题，本研究整合了不同植物演化支系——石松属（clubmosses）、卷柏属（spikemosses）、薄囊蕨类（leptosporangiate ferns）、瓶尔小草类蕨类（ophioglossioid ferns）、莲座蕨类蕨类（marattioid ferns）、松叶蕨类（whisk ferns）、木贼属（horsetails）以及松柏类（conifers）——中具有不同形态叶片的发育相关现有分子与结构数据。

具体而言，本研究探讨了叶片近-远轴、腹/背轴以及侧向发育的特性；叶肉分化为栅栏薄壁组织与海绵薄壁组织的有无情况；以及叶片维管束的类型（外韧维管束（collateral）与双韧维管束（bicollateral））。此外，我们结合产生叶原基（leaf primordia）的茎尖分生组织（shoot apical meristems, SAMs）——单原型（monoplex）、原型（simplex）或双原型（duplex）——的组织方式，分析了叶片发育的类群特异性与形态特异性特征。

现有数据表明，叶片起始的细胞模式与茎尖分生组织的结构显著相关，但与后续的叶片发育进程或最终形态无关联。叶片发育的后期阶段既与茎尖分生组织结构无关，也与类群分类无关。

本研究还讨论了被子植物中调控腹面（ARP与C3HDZ）和背面（YABBY与KANADI）叶片域发育，或建立叶片边缘分生组织（WOX）的同源基因的存在情况，以及其表达模式（若有可用数据）。研究发现，仅具有海绵组织而无栅栏组织的叶片（来自卷柏属、石松属、松叶蕨类、木贼属以及多数松柏类）与分化有栅栏与海绵组织的叶片（来自薄囊蕨类、银杏属、买麻藤属以及被子植物）之间，调控背腹叶片域发育的转录因子（transcription factors, TFs）同源基因集不存在相关性。

在叶片与孢子囊（sporangium）原基中均有表达的三类叶片发育调控因子（四类调控因子中的三类）——卷柏属与松叶蕨类中的C3HDZ、石松属中的YABBY，以及卷柏属与木贼属中的KANADI——表明，孢子囊发育程序可能被招募作为小型叶（microphylls）与大型叶（euphylls）起源的“前驱程序”。此外，在卷柏属（ARP、C3HDZ与KANADI）、石松属（YABBY）、薄囊蕨类（C3HDZ）以及木贼属（C3HDZ与KANADI）的茎尖分生组织中检测到的叶片发育调控因子的表达，表明至少部分茎尖分生组织调控机制也被招募至叶片前驱的预程序中。