Evolution and roles of cytokinin genes in angiosperms 2: Do ancient CKXs play housekeeping roles while non-ancient CKXs play regulatory roles?
Xiaojing Wang, Jing Ding, Shanshan Lin, Decai Liu, Tingting Gu, Han Wu, Robert N. Trigiano, Richard McAvoy, Jinling Huang, Yi Li
Abstract
Abstract Cytokinin oxidase/dehydrogenase (CKX) is a key enzyme responsible for the degradation of endogenous cytokinins. However, the origins and roles of CKX genes in angiosperm evolution remain unclear. Based on comprehensive bioinformatic and transgenic plant analyses, we demonstrate that the CKX s of land plants most likely originated from an ancient chlamydial endosymbiont during primary endosymbiosis. We refer to the CKX s retaining evolutionarily ancient characteristics as “ancient CKX s” and those that have expanded and functionally diverged in angiosperms as “non-ancient CKX s”. We show that the expression of some non-ancient CKX s is rapidly inducible within 15 min upon the dehydration of Arabidopsis , while the ancient CKX ( AtCKX7 ) is not drought responsive. Tobacco plants overexpressing a non-ancient CKX display improved oxidative and drought tolerance and root growth. Previous mutant studies have shown that non-ancient CKX s regulate organ development, particularly that of flowers. Furthermore, ancient CKXs preferentially degrade cis -zeatin ( c Z)-type cytokinins, while non-ancient CKXs preferentially target N 6 -(Δ 2 -isopentenyl) adenines (iPs) and trans -zeatins ( t Zs). Based on the results of this work, an accompanying study (Wang et al. 10.1038/s41438-019-0211-x ) and previous studies, we hypothesize that non-ancient CKXs and their preferred substrates of iP/ t Z-type cytokinins regulate angiosperm organ development and environmental stress responses, while ancient CKXs and their preferred substrates of c Zs play a housekeeping role, which echoes the conclusions and hypothesis described in the accompanying report (Wang, X. et al. Evolution and roles of cytokinin genes in angiosperms 1: Doancient IPTs play housekeeping while non-ancient IPTs play regulatory roles? Hortic Res 7 , (2020). 10.1038/s41438-019-0211-x ).