An ABA-serotonin module regulates root suberization and salinity tolerance.

Suberin in roots acts as a physical barrier preventing water/mineral losses. In Arabidopsis, root suberization is regulated by abscisic acid (ABA) and ethylene in response to nutrient stresses. ABA also mediates coordination between microbiota and root endodermis in mineral nutrient homeostasis. However, it is not known whether this regulatory system is common to plants in general, and whether there are other key molecule(s) involved. We show that serotonin acts downstream of ABA in regulating suberization in rice and Arabidopsis and negatively regulates suberization in rice roots in response to salinity. We show that ABA represses transcription of the key gene (OsT5H) in serotonin biosynthesis, thus promoting root suberization in rice. Conversely, overexpression of OsT5H or supplementation with exogenous serotonin represses suberization and reduces tolerance to salt stress. These results identify an ABA-serotonin regulatory module controlling root suberization in rice and Arabidopsis, which is likely to represent a general mechanism as ABA and serotonin are ubiquitous in plants. These findings are of significant importance to breeding novel crop varieties that are resilient to abiotic stresses and developing strategies for production of suberin-rich roots to sequestrate more CO2 , helping to mitigate the effects of climate change.

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

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.

A potassium-sensing niche in Arabidopsis roots orchestrates signaling and adaptation responses to maintain nutrient homeostasis.

Organismal homeostasis of the essential ion K+ requires sensing of its availability, efficient uptake, and defined distribution. Understanding plant K+ nutrition is essential to advance sustainable agriculture, but the mechanisms underlying K+ sensing and the orchestration of downstream responses have remained largely elusive. Here, we report where plants sense K+ deprivation and how this translates into spatially defined ROS signals to govern specific downstream responses. We define the organ-scale K+ pattern of roots and identify a postmeristematic K+-sensing niche (KSN) where rapid K+ decline and Ca2+ signals coincide. Moreover, we outline a bifurcating low-K+-signaling axis of CIF peptide-activated SGN3-LKS4/SGN1 receptor complexes that convey low-K+-triggered phosphorylation of the NADPH oxidases RBOHC, RBOHD, and RBOHF. The resulting ROS signals simultaneously convey HAK5 K+ uptake-transporter induction and accelerated Casparian strip maturation. Collectively, these mechanisms synchronize developmental differentiation and transcriptome reprogramming for maintaining K+ homeostasis and optimizing nutrient foraging by roots.

Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca2+ binding.

RBOHF from Arabidopsis thaliana represents a multifunctional NADPH oxidase regulating biotic and abiotic stress tolerance, developmental processes and guard cell aperture. The molecular components and mechanisms determining RBOHF activity remain to be elucidated. Here we combined protein interaction studies, biochemical and genetic approaches, and pathway reconstitution analyses to identify and characterize proteins that confer RBOHF regulation and elucidated mechanisms that adjust RBOHF activity. While the Ca2+ sensor-activated kinases CIPK11 and CIPK26 constitute alternative paths for RBOHF activation, the combined activity of CIPKs and the kinase open stomata 1 (OST1) triggers complementary activation of this NADPH oxidase, which is efficiently counteracted through dephosphorylation by the phosphatase ABI1. Within RBOHF, several distinct phosphorylation sites (p-sites) in the N-terminus of RBOHF appear to contribute individually to activity regulation. These findings identify RBOHF as a convergence point targeted by a complex regulatory network of kinases and phosphatases. We propose that this allows for fine-tuning of plant reactive oxygen species (ROS) production by RBOHF in response to different stimuli and in diverse physiological processes.

The calcineurin B-like Ca2+ sensors CBL1 and CBL9 function in pollen germination and pollen tube growth in Arabidopsis.

Ca(2+) has been established as an important second messenger regulating pollen germination and tube growth. However, to date, only a few signaling components have been identified to decode and relay Ca(2+) signals in growing pollen tubes. Here, we report a function for the calcineurin B-like (CBL) Ca(2+) sensor proteins CBL1 and CBL9 from Arabidopsis in pollen germination and tube growth. Both proteins are expressed in mature pollen and pollen tubes and impair pollen tube growth and morphology if transiently overexpressed in tobacco pollen. The induction of these phenotypes requires efficient plasma membrane targeting of CBL1 and is independent of Ca(2+) binding to the fourth EF-hand of CBL1. Overexpression of CBL1 or its closest homolog CBL9 in Arabidopsis renders pollen germination and tube growth hypersensitive towards high external K(+) concentrations while disruption of CBL1 and CBL9 reduces pollen tube growth under low K(+) conditions. Together, our data identify a crucial function for CBL1 and CBL9 in pollen germination and tube growth and suggest a model in which both proteins act at the plasma membrane through regulation of K(+) homeostasis.