Ikematsu Shuka, Umase Tatsushi, Shiozaki Mako, Nakayama Sodai, Noguchi Fuko, Sakamoto Tomoaki, Hou Hongwei, Gohari Gholamreza, Kimura Seisuke, Torii Keiko U
Faculty of Life Sciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-Ku, Kyoto 603-8555, Japan; Institute of Transformative Biomolecules (WPI-ITbM), Nagoya University, Chikusa, Nagoya, Aichi 464-8601, Japan; Center for Plant Sciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-Ku, Kyoto 603-8555, Japan.
Faculty of Life Sciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-Ku, Kyoto 603-8555, Japan.
Curr Biol. 2023 Feb 6;33(3):543-556.e4. doi: 10.1016/j.cub.2022.12.064. Epub 2023 Jan 24.
Land plants have evolved the ability to cope with submergence. Amphibious plants are adapted to both aerial and aquatic environments through phenotypic plasticity in leaf form and function, known as heterophylly. In general, underwater leaves of amphibious plants are devoid of stomata, yet their molecular regulatory mechanisms remain elusive. Using the emerging model of the Brassicaceae amphibious species Rorippa aquatica, we lay the foundation for the molecular physiological basis of the submergence-triggered inhibition of stomatal development. A series of temperature shift experiments showed that submergence-induced inhibition of stomatal development is largely uncoupled from morphological heterophylly and likely regulated by independent pathways. Submergence-responsive transcriptome analysis revealed rapid reprogramming of gene expression, exemplified by the suppression of RaSPEECHLESS and RaMUTE within 1 h and the involvement of light and hormones in the developmental switch from terrestrial to submerged leaves. Further physiological studies place ethylene as a central regulator of the submergence-triggered inhibition of stomatal development. Surprisingly, red and blue light have opposing functions in this process: blue light promotes, whereas red light inhibits stomatal development, through influencing the ethylene pathway. Finally, jasmonic acid counteracts the inhibition of stomatal development, which can be attenuated by the red light. The actions and interactions of light and hormone pathways in regulating stomatal development in R. aquatica are different from those in the terrestrial species, Arabidopsis thaliana. Thus, our work suggests that extensive rewiring events of red light to ethylene signaling might underlie the evolutionary adaption to water environment in Brassicaceae.
陆地植物已经进化出应对水淹的能力。两栖植物通过叶片形态和功能的表型可塑性，即异形叶性，来适应陆生和水生环境。一般来说，两栖植物的水下叶片没有气孔，但其分子调控机制仍不清楚。利用十字花科两栖物种水杨梅（Rorippa aquatica）这一新兴模型，我们为水淹触发的气孔发育抑制的分子生理基础奠定了基础。一系列温度转换实验表明，水淹诱导的气孔发育抑制在很大程度上与形态异形叶性无关，可能由独立的途径调控。水淹响应转录组分析揭示了基因表达的快速重编程，例如在1小时内RaSPEECHLESS和RaMUTE受到抑制，以及光和激素参与从陆生叶到水下叶的发育转变。进一步的生理研究表明乙烯是水淹触发的气孔发育抑制的核心调节因子。令人惊讶的是，红光和蓝光在此过程中具有相反的作用：蓝光促进气孔发育，而红光通过影响乙烯途径抑制气孔发育。最后，茉莉酸抵消了气孔发育的抑制作用，而红光可以减弱这种作用。水杨梅中光和激素途径在调节气孔发育中的作用和相互作用与陆生植物拟南芥不同。因此，我们的研究表明，红光到乙烯信号的广泛重布线事件可能是十字花科植物对水环境进化适应的基础。
