Suberin plasticity to developmental and exogenous cues is regulated by a set of MYB transcription factors

Abstract

Suberin is a hydrophobic biopolymer that can be deposited at the periphery of cells, forming protective barriers against biotic and abiotic stress. In roots, suberin forms lamellae at the periphery of endodermal cells where it plays crucial roles in the control of water and mineral transport. Suberin formation is highly regulated by developmental and environmental cues. However, the mechanisms controlling its spatiotemporal regulation are poorly understood. Here, we show that endodermal suberin is regulated independently by developmental and exogenous signals to fine-tune suberin deposition in roots. We found a set of four MYB transcription factors (MYB41, MYB53, MYB92, and MYB93), each of which is individually regulated by these two signals and is sufficient to promote endodermal suberin. Mutation of these four transcription factors simultaneously through genome editing leads to a dramatic reduction in suberin formation in response to both developmental and environmental signals. Most suberin mutants analyzed at physiological levels are also affected in another endodermal barrier made of lignin (Casparian strips) through a compensatory mechanism. Through the functional analysis of these four MYBs, we generated plants allowing unbiased investigation of endodermal suberin function, without accounting for confounding effects due to Casparian strip defects, and were able to unravel specific roles of suberin in nutrient homeostasis.

The Key Enzymes in the Suberin Biosynthetic Pathway in Plants: An Update

“…Expectedly, the corresponding Arabidopsis atsub mutant roots accumulated less suberin content compared to wild-type roots [54]. More recently, Shukla et al [51] showed that MYB41, MYB53, MYB92 and MYB93 all promote endodermal suberization in Arabidopsis roots (Figure 3). The authors mutated these four MYBs simultaneously through genome-editing tools, which led to a dramatic reduction in suberin formation in response to both developmental and environmental signals [51].…”

Root Suberin Plays Important Roles in Reducing Water Loss and Sodium Uptake in Arabidopsis thaliana

“…Therefore, we investigated their suberin composition and lamellae structure. Of note, a recent study reported the suberin composition of myb41 myb53 myb92 myb93, a quadruple mutant that shows an overall ~78% decrease in suberin monomers compared to the wild type [30].…”

“…Compared to the wild type, esb1 has higher water-use efficiency (WUE) and a lower transpiration rate associated with enhanced suberin deposition in roots [28]. Conversely, suberin-deficient mutants show susceptibility to salt stress [24,29,30]. In a recent study, suberin deposition was characterized through development and found to be upregulated under water-deficit conditions in grapevine roots [31].…”

Role of Basal ABA in Plant Growth and Development

“…Several studies have shown that exogenous application of ABA induces the expression of suberin-related genes and increases suberin deposition in the endodermis, while triggering ectopic suberin deposition in root tips and in potato tubers [ 76 , 154 , 155 , 156 , 157 , 158 , 159 ]. An essential role of basal ABA in endodermal suberization has been supported by genetic studies.…”

“…ABA-dependent suberin deposition is mediated by MYB41-MYB53-MYB92-MYB93 , which are expressed in the endodermis and induced by ABA. A quadruple myb41 myb53 myb92 myb93 mutant shows a nearly complete lack of endodermal root suberin, which could not be rescued by application of ABA [ 159 ], whereas overexpression of some MYB TFs results in ectopic suberin accumulation [ 156 , 160 ] ( Figure 2 ). ABA-induced suberin deposition also requires the auxin-regulated GDSL lipases, some of which have been proposed to be involved in suberin degradation while other in ABA-mediated suberin synthesis [ 159 ].…”