SUBERMAN regulates developmental suberization of the Arabidopsis root endodermis

Abstract

SummaryRoot endodermis, the innermost cortical layer surrounding the root vasculature, serves as the foremost barrier to water, solutes, and nutrients taken up from soil. Endodermis barrier functionality is achieved via its hydrophobic coating of lignified Casparian strips and the suberin lamellae; nonetheless the regulatory mechanisms underlying endodermis suberization are still elusive. Here, we discovered that the Arabidopsis SUBERMAN (SUB) transcription factor controls the establishment of the root suberin lamellae. Transient expression of SUB in Nicotiana benthamiana leaves resulted in the induction of heterologous suberin genes, the accumulation of suberin‐type monomers, and consequent deposition of suberin‐like lamellae. We demonstrate that SUB exerts its regulatory roles by transactivating promoters of suberin genes. In Arabidopsis, SUB is expressed in patchy and continuous suberization root endodermal cells, and thus roots with higher or lower expression of SUB display altered suberin polymer deposition patterns and modified composition. While these changes did not interfere with Casparian strip formation they had a substantial effect on root uptake capacity, resulting in varied root and leaf ionomic phenotypes. Gene expression profiling revealed that SUB function impacts transcriptional networks associated with suberin, phenylpropanoids, lignin, and cuticular lipid biosynthesis, as well as root transport activities, hormone signalling, and cell wall modification. Our findings highlight SUB as a regulator of root endodermis suberization during normal development, and its characterization is thus a key step towards dissecting the molecular mechanisms partaking in root endodermal barrier functionalities.

Drought activates MYB41 orthologs and induces suberization of grapevine fine roots

“…The induction of suberization by abscisic acid was reported decades ago (Cottle & Kolattukudy, 1982), while its repression by ethylene was recently suggested (Barberon et al, 2016). The direct activation of several suberin-biosynthesis genes by MYB transcription factors has been reported for QsMYB1, AtMYB39, AtMYB92, and AtMYB107 (Capote et al, 2018;Cohen et al, 2020;Gou et al, 2017;To et al, 2020). Recently in kiwifruits, Wei and coworkers showed that abscisic acid induced the expression of AchnMYB41 which upregulated downstream suberin-related genes .…”

“…Interestingly, individual MYBs appear to differently affect specific organs in Arabidopsis. For example, AtMYB107 specifically affects seed coat suberin while AtMYB39 primarily affects root suberin (Cohen et al, 2020;Gou et al, 2017). In addition to MYBs, NAC transcription factors were shown to activate or repress suberization (Mahmood et al, 2019;Soler et al, 2020;Verdaguer et al, 2016).…”

“…Additionally, BAHD-acyl transferase like aliphatic suberin feruloyl transferase (ASFT) are important for the incorporation of hydroxycinnamic acids in the polymer (Molina et al, 2009). Finally, at the level of transcriptional regulation several MYB transcription factors (AtMYB9, AtMYB39, AtMYB41, AtMYB92, and AtMYB107) have been shown to be important positive regulators of suberin biosynthesis in Arabidopsis (Cohen et al, 2020;Gou et al, 2017;Kosma et al, 2014;Lashbrooke et al, 2016;To et al, 2020). Other suberin transcriptional regulators were also identified in oak cork (Capote et al, 2018), potato periderm (Soler et al, 2020;Verdaguer et al, 2016), and russeted apple skins (Legay et al, 2016).…”

GDSL-domain containing proteins mediate suberin biosynthesis and degradation, enabling developmental plasticity of the endodermis during lateral root emergence

“…Although the Arabidopsis genome contains more than 100 GDSL-domain containing genes, only a few of them have been functionally linked to cell wall modification or have been demonstrated to be able to synthesize or degrade cell wall polymers (Naseer et al, 2012;Philippe et al, 2020;Yeats et al, 2012). Several suberin biosynthetic genes as well as transcriptional regulators have been identified in recent years (Beisson et al, 2007;Cohen et al, 2020;Kosma et al, 2014;Yadav et al, 2014). Although suberin is chemically similar to cutin, there are significant differences in its composition and its deposition within the cell wall and we still do not know how suberin is polymerized and degraded.…”

An Arabidopsis gene expression predictor enables inference of transcriptional regulators

“…Under such criterion, 27 TFs, including MYB41, were identified as predictor TFs for Module #84, among which are known suberin regulators like MYB41, MYB107, MYB9 (17,18), and other MYB-, NAC-, and WRKY-type TFs as potential regulators ( Figure 4B). Interestingly, among the potential regulators, MYB39 was recently shown to be another regulator of suberization (20).…”