Evolution and roles of cytokinin genes in angiosperms 1: Do ancient IPTs play housekeeping while non-ancient IPTs play regulatory roles?

Abstract

Isopentenyltransferase (IPT) genes, including those encoding ATP/ADP-IPTs and tRNA-IPTs, control the rate-limiting steps of the biosynthesis of N 6-(Δ 2-isopentenyl)adenine (iP)-type and trans-zeatin (tZ)-type cytokinins and cis-zeatin (cZ)-type cytokinins, respectively. However, the evolution and roles of these IPTs in angiosperms are not well understood. Here, we report comprehensive analyses of the origins, evolution, expression patterns, and possible roles of ATP/ADP-IPTs and tRNA-IPTs in angiosperms. We found that Class I and II tRNA-IPTs likely coexisted in the last common ancestor of eukaryotes, while ATP/ADP-IPTs likely originated from a Class II tRNA-IPT before the divergence of angiosperms. tRNA-IPTs are conservatively retained as 2-3 copies, but ATP/ADP-IPTs exhibit considerable expansion and diversification. Additionally, tRNA-IPTs are constitutively expressed throughout the plant, whereas the expression of ATP/ADP-IPTs is tissue-specific and rapidly downregulated by abiotic stresses. Furthermore, previous studies and our present study indicate that ATP/ADP-IPTs and their products, iPs/tZs, may regulate responses to environmental stresses and organ development in angiosperms. We therefore hypothesize that tRNA-IPTs and the associated cZs play a housekeeping role, whereas ATP/ADP-IPTs and the associated iP/tZ-type cytokinins play regulatory roles in organ development and stress responses in angiosperms, which echoes the conclusions and hypothesis presented in the accompanying study by Wang, X. et al Evolution and roles of cytokinin genes in angiosperms 2: Do ancient CKXs play housekeeping roles while non-ancient CKXs play regulatory roles? Hortic Res

Evolution and roles of cytokinin genes in angiosperms 2: Do ancient CKXs play housekeeping roles while non-ancient CKXs play regulatory roles?

“…In conclusion, based on the results from the accompanying (Wang et al 36 ) and the current studies, we propose that in angiosperms, the ancient tRNA-IPTs and CKXs and their products or preferred substrates, the cZtype cytokinins, play a housekeeping role to maintain basic cellular functions. On the other hand, the nonancient ATP/ADP-IPTs and CKXs and their products or preferred substrates, the iP-and tZ-type cytokinins, contribute more to the regulation of organ development and abiotic stress responses.…”

“…There are two types of IPT genes, tRNA-IPTs (ancient cytokinin biosynthesis genes) and ATP/ADP-IPTs (nonancient cytokinin biosynthesis genes), in angiosperms. In an accompanying article on this topic (Wang et al 36 ), we show that in angiosperms, the tRNA-IPT (ancient) genes are conservatively retained, constitutively expressed throughout the plant, and nonresponsive or only slightly responsive to environmental stresses. On the other hand, the expression of ATP/ADP-IPTs (non-ancient), which emerged and diverged in angiosperms, is tissue specific and is rapidly downregulated under various stress conditions.…”

“…It is particularly interesting that we found similar characteristics between the ancient/non-ancient CKX genes and the ancient/non-ancient IPT (tRNA-type and ATP/ADP-type) genes in terms of their evolution, tissue/ organ expression and environmental stress responses in angiosperms ( Table 2). Based on several lines of evidence discussed below, we hypothesize that, similar to the ATP/ ADP-IPT (non-ancient) genes (Wang et al 36 ), the nonancient CKXs play regulatory roles in organ development and the adaption of angiosperms to environmental stresses, whereas the ancient CKXs more likely exhibit housekeeping functions, similar to the tRNA-IPT (ancient) genes.…”

“…Experiments in CKX-overexpressing plants also show that the non-ancient AtCKXs degrade tZs much more efficiently than the ancient AtCKX7, whereas AtCKX7 preferentially degrades cZs 13 . We have proposed the hypothesis in the accompanying article in this issue (Wang et al 36 ) that iPs/tZs play more regulatory roles in organ development and stress responses, while cZs play a housekeeping role in maintaining basic cellular functions, based on the analyses of the corresponding genes responsible for their biosynthesis (ATP/ADP-IPTs and tRNA-IPTs). In this study, we provide further supporting evidence for this hypothesis from comparative analyses of non-ancient and ancient CKXs ( Table 2).…”

Comparative Transcriptomic Analysis of the Development of Sepal Morphology in Tomato (Solanum Lycopersicum L.)

“…In angiosperms, the ancient tRNA-IPTs and CKXs preferred the cZtype cytokinins as substrates, play a housekeeping role to maintain basic cellular functions. On the other hand, the nonancient ATP/ADP-IPTs and CKXs preferred the iP-and tZ-type cytokinins as bstrates, contribute more to the regulation of organ development and abiotic stress responses [83]. Five zeatin O-glucosyltransferase and zeatin O-xylosyltransferase (cisZOG) genes were upregulated 3.46 fold to 1.67-fold.…”