A phospho-switch provided by LRR receptor-like kinase, ALK1/QSK1/KIN7, prioritizes ABCG36/PEN3/PDR8 transport toward defense

Abstract

Based on its proposed substrate preferences, the ABC transporter, ABCG36/PDR8/PEN3, from the model plant Arabidopsis stands at the cross-road between growth and defence. Recently, ABCG36 was shown to export a few indolic compounds, including the auxin precursor, indole-3-butyric acid (IBA), and to be implicated in the export of the major phytoalexin of Arabidopsis, camalexin, although clear-cut proof of camalexin transport activity is still lacking.Here we provide strong evidence that ABCG36 catalyses the direct, ATP-dependent export of camalexin over the plasma membrane, however, most likely in functional interplay with non-camalexin transporting ABCG isoforms. We identify the leucin-rich repeat receptor-like kinase, Auxin-induced LRR Kinase1 (ALK1/KIN7/QSK1), as a functional kinase to physically interact with and phosphorylate ABCG36. ABCG36 phosphorylation by ALK1 represses unilaterally IBA but not camalexin export leading to a prioritization of ABCG transport toward defense. As a consequence, phospho-dead mutants of ABCG36, like alk1 and abcg36 alleles, are hypersensitive toward infection with the root pathogen, F. oxysporum, caused by elevated fungal progression.Our findings indicate a novel, direct regulatory circuit between a receptor kinase and an ABC transporter determining transporter substrate specificity. It appears that growth and defense balance decisions in plants are performed on the transporter level by means of a reversible phospho-switch.

Protein Phosphorylation Orchestrates Acclimations ofArabidopsisPlants to Environmental pH

“…In PDR8, a close homolog of PDR7 (83% identity), phosphorylation represses the transport of indole-3-butyric acid (IBA) on the expense of camalexin, thereby prioritizing defense over growth. Here, S823 and S825 serves as phospho-switches (29). A similar phospho-switch may alter substrate specificity of PDR7, prioritizing defense over growth at low pH.…”

“…Post-translational modifications of this type of transporters not only change their activity, but may also have consequences for their substrate specificity. For instance, PDR8 prioritizes either IBA or camalexin transport, a discretion governed by the phosphorylation state of the transporter (29). In the case of PDR8, phosphorylation - mediated by the LRR receptor-like kinase KIN7 - decreases the efflux of the ‘canonical’ substrate IBA and, as a consequence, favors the export of the phytoalexin camalexin (29).…”

“…For instance, PDR8 prioritizes either IBA or camalexin transport, a discretion governed by the phosphorylation state of the transporter (29). In the case of PDR8, phosphorylation - mediated by the LRR receptor-like kinase KIN7 - decreases the efflux of the ‘canonical’ substrate IBA and, as a consequence, favors the export of the phytoalexin camalexin (29). The phosphorylation sites of PDR8 are arranged in two clusters (cluster 1: S40 and S45; cluster 2: S823 and S825) preceding the nucleotide binding domains (29).…”

“…In the case of PDR8, phosphorylation - mediated by the LRR receptor-like kinase KIN7 - decreases the efflux of the ‘canonical’ substrate IBA and, as a consequence, favors the export of the phytoalexin camalexin (29). The phosphorylation sites of PDR8 are arranged in two clusters (cluster 1: S40 and S45; cluster 2: S823 and S825) preceding the nucleotide binding domains (29). Phosphorylation of PDR8 at S45 decreased in pH 7.5 plants, indicating that IBA export and, thus, growth is favored under these conditions.…”