GSK3 activity is a cell fate switch that balances the ratio of vascular cell type

Abstract

The phloem transports photosynthetic assimilates and signalling molecules. It mainly consists of sieve elements (SEs), which act as "highways" for transport, and companion cells (CCs), which serve as "gates" to load/unload cargos. Though SEs and CCs function together, it remains unknown what determines the ratio of SE /CC in the phloem. In this study, we develop a novel culture system for CC differentiation named VISUAL-CC, which reconstitutes the SE-CC complex formation. Comparative expression analysis in VISUAL-CC reveals that SE and CC differentiation tends to show negative correlation, while total phloem differentiation is unchanged. This varying SE/CC ratio is largely dependent on GSK3 kinase activity. Indeed, gsk3 hextuple mutants possess much more SEs and less CCs in planta. Conversely, gsk3 gain-of-function mutants induced by phloem-specific promoter partially increased the CC ratio. Taken together, GSK3 activity appears to function as a cell fate switch in the phloem, thereby balancing the SE/CC ratio.

Regulatory network of GSK3-like kinases and their role in plant stress response

“…The bin2 bil1 bil2 triple mutants showed a constitutive BR-activation phenotype (Yan et al, 2009). The BR signaling has been well elucidated and proved to be an important regulator of plant physiological and biological processes including seed germination, cell division, elongation and differentiation, leaf senescence and response to biotic and abiotic stresses (Rozhon et al, 2010;Kondo et al, 2014;Dong et al, 2015;Anwar et al, 2018;Peres et al, 2019;Ackerman-Lavert and Savaldi-Goldstein, 2020;Tamaki et al, 2020;Zolkiewicz and Gruszka, 2022). BRs are recognized by the leucine-rich repeat receptor-like (LRR-RLK) protein brassinosteroid-insensitive 1 (BRI1) and its co-receptor BRI1 associated receptor kinase 1 (BAK1) at the membrane (Wang et al, 2008;Santiago et al, 2013).…”

“…A series of GSK3s proteins, such as AtBIN2, AtBIL1, AtBIL2, AtSK11, AtSK12, OsGSK2, and TaSG-D1, is degradated through proteasome-mediated pathway (Li and Nam, 2002;Peng et al, 2008;Yan et al, 2009;Tong et al, 2012;Li et al, 2018;Cheng et al, 2020;Chen et al, 2020b). Moreover, the proteasome-mediated regulation of GSK3s is modulated via a conserved C-terminal TREE motif, and mutations in this motif Kondo et al, 2014;Tamaki et al, 2020;Li et al, 2018;Chen et al, 2020b;Stampfl et al, 2016;Dong et al, 2020;Dal Santo et al, 2012 II AtSK21, AtSK22, AtSK23 BR signal/Growth/Salt stress Li and Nam, 2002;Yan et al, 2009; Yang et al, 2016;Xiao et al, 2017;Gao et al, 2019;Min et al, 2019;Lyu et al, 2020;Xiao et al, 2020;Sun et al, 2015;Sun et al, 2018;Che et al, 2015;Liu et al, 2017;Koh et al, 2007;…”

A morpho-transcriptomic map of brassinosteroid action in the Arabidopsis root

“…Because brassinosteroid biosynthesis is a branched pathway (Ohnishi et al, 2006), and because brassinosteroid signaling is subject to negative feedbacks (Ruan et al, 2018; and can additionally act through non-canonical outputs (Caesar et al, 2011;Cho et al, 2014;Holzwart et al, 2018;Kondo et al, 2014;Tamaki et al, 2020;Wolf et al, 2014), the brassinosteroid receptor triple null mutant represents the consequences of absent brassinosteroid action most stringently. We therefore concentrated our efforts on the bri TRIPLE mutant and contrasted it against wildtype and bri TRIPLE mutants in which brassinosteroid signaling was exclusive restored in the developing protophloem sieve elements ("bri T-RESCUE ") (Graeff et al, 2020;Kang et al, 2017).…”

“…Yet detailed analysis of a biosynthesis mutant suggests that brassinosteroids promote the exit from cell division, and thereby also the transition to cell expansion and differentiation (Zhiponova et al, 2013). Moreover, it has been proposed that brassinosteroid signaling is required for the differentiation of vascular tissues (Cano-Delgado et al, 2004;Holzwart et al, 2018;Kang et al, 2017;Tamaki et al, 2020;Yamamoto et al, 2001).…”