Ministry of Education Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, Hebei 050024, China; Hebei Research Center of the Basic Discipline of Cell Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, Hebei 050024, China; Hebei Collaboration Innovation Center for Cell Signaling and Environmental Adaptation, College of Life Sciences, Hebei Normal University, Shijiazhuang, Hebei 050024, China; Hebei Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, Hebei 050024, China.
State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, Hebei 050021, China.
Plant Commun. 2024 Jun 10;5(6):100850. doi: 10.1016/j.xplc.2024.100850. Epub 2024 Feb 25.
After germination in the dark, plants produce a shoot apical hook and closed cotyledons to protect the quiescent shoot apical meristem (SAM), which is critical for seedling survival during skotomorphogenesis. The factors that coordinate these processes, particularly SAM repression, remain enigmatic. Plant cuticles, multilayered structures of lipid components on the outermost surface of the aerial epidermis of all land plants, provide protection against desiccation and external environmental stresses. Whether and how cuticles regulate plant development are still unclear. Here, we demonstrate that mutants of BODYGUARD1 (BDG1) and long-chain acyl-CoA synthetase2 (LACS2), key genes involved in cutin biosynthesis, produce a short hypocotyl with an opened apical hook and cotyledons in which the SAM is activated during skotomorphogenesis. Light signaling represses expression of BDG1 and LACS2, as well as cutin biosynthesis. Transcriptome analysis revealed that cuticles are critical for skotomorphogenesis, particularly for the development and function of chloroplasts. Genetic and molecular analyses showed that decreased HOOKLESS1 expression results in apical hook opening in the mutants. When hypoxia-induced expression of LITTLE ZIPPER2 at the SAM promotes organ initiation in the mutants, the de-repressed expression of cell-cycle genes and the cytokinin response induce the growth of true leaves. Our results reveal previously unrecognized developmental functions of the plant cuticle during skotomorphogenesis and demonstrate a mechanism by which light initiates photomorphogenesis through dynamic regulation of cuticle synthesis to induce coordinated and systemic changes in organ development and growth during the skotomorphogenesis-to-photomorphogenesis transition.
在黑暗中发芽后，植物会产生一个芽尖钩和闭合的子叶，以保护休眠的芽尖分生组织（SAM），这对于种子在暗中形态发生过程中的生存至关重要。协调这些过程的因素，特别是 SAM 的抑制，仍然是个谜。植物角质层是所有陆生植物气生表皮最外层的多层脂质成分结构，提供了对干燥和外部环境胁迫的保护。角质层是否以及如何调节植物发育尚不清楚。在这里，我们证明了参与角质生物合成的关键基因 BODYGUARD1 (BDG1) 和长链酰基辅酶 A 合成酶 2 (LACS2) 的突变体在暗中形态发生过程中产生了一个短的下胚轴，带有一个打开的顶端钩和子叶，其中 SAM 被激活。光信号抑制 BDG1 和 LACS2 的表达以及角质的生物合成。转录组分析表明，角质层对于暗中形态发生至关重要，特别是对于叶绿体的发育和功能。遗传和分子分析表明，HOOKLESS1 表达的减少导致突变体中顶端钩的打开。当 SAM 中缺氧诱导的 LITTLE ZIPPER2 的表达促进突变体中器官的起始时，细胞周期基因去抑制表达和细胞分裂素反应诱导真叶的生长。我们的研究结果揭示了植物角质层在暗中形态发生过程中的先前未被识别的发育功能，并证明了光通过动态调节角质层合成来启动光形态发生的机制，从而在暗中形态发生到光形态发生的转变过程中诱导器官发育和生长的协调和系统变化。
