Suppression of Leaf Blade Development by BLADE-ON-PETIOLE Orthologs Is a Common Strategy for Underground Rhizome Growth

First author: Taiyo Toriba; Affiliations: Tohoku University (东北大学): Sendai, Japan

Corresponding author: Junko Kyozuka

Rhizomes are modified stems that grow horizontally underground in various perennial species, a growth habit that is advantageous for vigorous asexual proliferation. In Oryza longistaminata, a rhizomatous wild relative of cultivated rice (Oryza sativa), leaves in the aerial shoots consist of a distal leaf blade and a proximal leaf sheath. Leaf blade formation is, however, suppressed in rhizome leaves. In O. sativa, BLADE-ON-PETIOLE (BOP) genes are the main regulators of proximal-distal leaf patterning. During the juvenile phase of O. sativa, BOP expression is maintained at high levels by the small regulatory RNA microRNA156 (miR156), leading to formation of leaves consisting predominantly of the sheath. Here, we show that in O. longistaminata, high expression of BOPs caused by miR156 was responsible for suppression of the blade in rhizomes and that bop loss-of-function mutants produced leaves consisting of the leaf blade only. Rhizome growth in soil was also hampered in the mutants due to a severe reduction in rhizome tip stiffness. Leaf blade formation is also suppressed in the stolons of Zoysia matrella, a monocot species, and in the rhizomes of Houttuynia cordata, a dicot species, indicating that leaf blade suppression is widely conserved. We also show that strong expression of BOP homologs in both rhizome and stolon leaves rather than in aerial leaves is another conserved feature. We propose that suppression of the leaf blade by BOP is an evolutionary strategy that has been commonly recruited by both rhizomatous and stoloniferous species to establish their unique growth habit.

各种多年生物种的根茎是修饰后的茎，可以在地下水平生长，这种生长习性有利于旺盛的无性繁殖。栽培种水稻的野生近缘种长雄野生稻具有根茎，其地上部分组织的叶由一个远端叶片和一个近端叶鞘组成。叶片的形成在根茎中是被抑制的。在栽培种水稻中，BOP基因是近端-远端轴模式建成的主要调控因子。在水稻的幼年期，miR156将BOP基因的表达保持在较高的水平，从而形成了主要由叶鞘组成的叶。本文中，作者发现在长雄野生稻中，miR156诱导的BOP高表达是根茎中抑制叶片形成的主要原因，bop功能缺失突变体产生的叶只包含有叶片。突变体根茎顶端的硬度降低，所以在土壤中的生长有缺陷。在单子叶植物细叶结缕草的匍匐茎和双子叶植物鱼腥草的根茎中，叶片的形成也受到了抑制，表明叶片形成的抑制机制在单、双子叶植物中高度保守。作者的研究还发现了另一个保守的特征，即在匍匐茎和根茎中的BOP同源基因的表达量要比地上部分叶组织要高很多。作者认为BOP介导的叶片形成抑制是一种演化策略，根茎和匍匐茎植物广泛采用这种策略来建立其独特的生长习性。

通讯：Junko Kyozuka  (https://www.lifesci.tohoku.ac.jp/en/research/teacher/detail.html?id=33615)

个人简介：东京大学，学士；东京大学，硕士；澳大利亚CSIRO，博士。

研究方向：植物生长方式。

doi: https://doi.org/10.1016/j.cub.2019.11.055

Journal: Current Biology

Published date: January 16, 2020