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 CKXs of land plants most likely originated from an ancient chlamydial endosymbiont during primary endosymbiosis. We refer to the CKXs retaining evolutionarily ancient characteristics as “ancient CKXs” and those that have expanded and functionally diverged in angiosperms as “non-ancient CKXs”. We show that the expression of some non-ancient CKXs 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 CKXs regulate organ development, particularly that of flowers. Furthermore, ancient CKXs preferentially degrade cis-zeatin (cZ)-type cytokinins, while non-ancient CKXs preferentially target N6-(Δ2-isopentenyl) adenines (iPs) and trans-zeatins (tZs). Based on the results of this work, an accompanying study (Wang et al. https://doi.org/10.1038/s41438-019-0211-x) and previous studies, we hypothesize that non-ancient CKXs and their preferred substrates of iP/tZ-type cytokinins regulate angiosperm organ development and environmental stress responses, while ancient CKXs and their preferred substrates of cZs 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 Res7, (2020). https://doi.org/10.1038/s41438-019-0211-x).
Highlights
Cytokinins are a major class of hormones that regulate many developmental processes in plants, including cell division, shoot and root growth, and vascular and gametophyte development[1]
To systematically investigate the taxonomic distribution of cytokinin oxidases/dehydrogenases (CKXs) genes, we first conducted exhaustive HMMER, BLASTP, or TBLASTN searches for the Cytokin-bind domain (Pfam: PF09265), which is characteristic of CKX proteins, in organisms outside of land plants and bacteria
CKX genes were identified in all available complete proteomes of land plants (Table S3)
Summary
Cytokinins are a major class of hormones that regulate many developmental processes in plants, including cell division, shoot and root growth, and vascular and gametophyte development[1]. Natural cytokinins are N6-substituted adenine derivatives, and their most common forms in plants are N6-(Δ2-isopentenyl) adenines (iPs), trans-zeatins (tZs), and cis-zeatins (cZs). These cytokinin forms exhibit different levels of physiological activity and are differentially distributed among land plant lineages and in various tissues or stages of angiosperms[2]. The ATP/ADP- and tRNA-IPT genes encode the main enzymes responsible for the biosynthesis of tZ- and cZ-type cytokinins in angiosperms, respectively[5]. Only tRNA-IPT genes have been identified in seedless plants[8], and ATP/ADP-IPT genes are proposed to have arisen during the evolution of angiosperms, probably due to the need for higher levels of cytokinins[4]
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