Innovation, conservation, and repurposing of gene function in root cell type development Graphical abstract Highlights d Tomato cell type-resolution translatome atlas reveals cell type function d Conservation and repurposing in gene regulation between Arabidopsis and tomato d The tomato exodermis is lignified, suberized, and enriched for nitrogen regulation d The root meristem is molecularly homologous across plant species

HighlightMaturation of GLV signaling peptides requires two SBT6 subtilases. SBT6 proteolytic activity is further regulated by the Serpin1 inhibitor, implying a complex network that controls cell elongation in Arabidopsis.

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Nutrient availability and salinity of the soil affect the growth and development of plant roots. Here, we describe how inorganic phosphate (Pi) availability affects the root system architecture (RSA) of Arabidopsis (Arabidopsis thaliana) and how Pi levels modulate responses of the root to salt stress. Pi starvation reduced main root length and increased the number of lateral roots of Arabidopsis Columbia-0 seedlings. In combination with salt, low Pi dampened the inhibiting effect of mild salt stress (75 mM) on all measured RSA components. At higher salt concentrations, the Pi deprivation response prevailed over the salt stress only for lateral root elongation. The Pi deprivation response of lateral roots appeared to be oppositely affected by abscisic acid signaling compared with the salt stress response. Natural variation in the response to the combination treatment of salt and Pi starvation within 330 Arabidopsis accessions could be grouped into four response patterns. When exposed to double stress, in general, lateral roots prioritized responses to salt, while the effect on main root traits was additive. Interestingly, these patterns were not identical for all accessions studied, and multiple strategies to integrate the signals from Pi deprivation and salinity were identified. By genome-wide association mapping, 12 genomic loci were identified as putative factors integrating responses to salt stress and Pi starvation. From our experiments, we conclude that Pi starvation interferes with salt responses mainly at the level of lateral roots and that large natural variation exists in the available genetic repertoire of accessions to handle the combination of stresses.

ABSTRACT

Defects in RNA processing and degradation pathways often lead to developmental abnormalities, impaired hormonal signaling and altered resistance to abiotic and biotic stress. Here we report that components of the 5′-3′ mRNA decay pathway, DCP5, LSM1-7 and XRN4, contribute to a proper response to a key plant hormone abscisc acid (ABA), albeit in a different manner. Plants lacking DCP5 are more sensitive to ABA during germination, whereas lsm1a lsm1b and xrn4-5 mutants are affected at the early stages of vegetative growth. In addition, we show that DCP5 and LSM1 regulate mRNA stability and act in translational repression of the main components of the early ABA signaling, PYR/PYL ABA receptors and SnRK2s protein kinases. mRNA decapping DCP and LSM1-7 complexes also appear to modulate ABA-dependent expression of stress related transcription factors from the AP2/ERF/DREB family that in turn affect the level of genes regulated by the PYL/PYR/RCAR-PP2C-SnRK2 pathway. These observations suggest that ABA signaling through PYL/PYR/RCAR receptors and SnRK2s kinases is regulated directly and indirectly by the cytoplasmic mRNA decay pathway.

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Plant acclimation to environmental stresses requires fast signaling to initiate changes in developmental and metabolic responses. Regulation of gene expression by transcription factors and protein kinases acting upstream are important elements of responses to salt and drought. Gene expression can be also controlled at the post-transcriptional level. Recent analyses on mutants in mRNA metabolism factors suggest their contribution to stress signaling. Here we highlight the components of mRNA decay pathways that contribute to responses to osmotic and salt stress. We hypothesize that phosphorylation state of proteins involved in mRNA decapping affect their substrate specificity.