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The interaction of plant roots with bacteria is influenced by chemical signaling, where auxins play a critical role. Auxins exert positive or negative influences on the plant traits responsible of root architecture configuration such as root elongation and branching and root hair formation, but how bacteria that modify the plant auxin response promote or repress growth, as well as root structure, remains unknown. Here, we isolated and identified via molecular and electronic microscopy analysis a Micrococcus luteus LS570 strain as a plant growth promoter that halts primary root elongation in Arabidopsis seedlings and strongly triggers root branching and absorptive potential. The root biomass was exacerbated following root contact with bacterial streaks, and this correlated with inducible expression of auxin-related gene markers DR5:GUS and DR5:GFP. Cellular and structural analyses of root growth zones indicated that the bacterium inhibits both cell division and elongation within primary root tips, disrupting apical dominance, and as a consequence differentiation programs at the pericycle and epidermis, respectively, triggers the formation of longer and denser lateral roots and root hairs. Using Arabidopsis mutants defective on auxin signaling elements, our study uncovers a critical role of the auxin response factors ARF7 and ARF19, and canonical auxin receptors in mediating both the primary root and lateral root response to M. luteus LS570. Our report provides very basic information into how actinobacteria interact with plants and direct evidence that the bacterial genus Micrococcus influences the cellular and physiological plant programs ultimately responsible of biomass partitioning.

The RNA polymerase II drives the biogenesis of coding and non-coding RNAs for gene expression. Here, we describe new roles for its second-largest subunit, NRPB2, on root organogenesis and regeneration. Down-regulation of NRPB2 activates a determinate developmental program, which correlated with a reduction in mitotic activity, cell elongation, and size of the root apical meristem. Noteworthy, nrpb2-3 mutants manifest cell death in pro-vascular cells within primary root tips of plants grown in darkness or exposed to light, which triggers the expression of the regeneration gene marker ERF115 in neighbor cells close to damage. Auxin and stem cell niche (SCN) gene expression as well as structural analysis revealed that NRPB2 maintains SCN activity through distribution of PIN transporters in root tissues. Wild-type seedlings regenerated the root tip after excision of the QC and SCN, but nrpb2-3 mutants did not rebuild the missing tissues, and this process could be genotypified using pERF115:GFP, DR5:GFP, and pWOX5:GFP reporter constructs. The levels of reactive oxygen species increased in the mutants four days after germination and strongly decreased at later times, whereas nitric oxide accumulated as the root tip differentiates. These results show the importance of the transcriptional machinery for root organogenesis, cell viability, and regenerative capacity for reconstruction of tissues and organs upon injury.

Chemical communication underlies major adaptive traits in plants and shapes the root microbiome. An increasing number of diffusible and/or volatile organic compounds released by bacteria have been identified, which play phytostimulant or protective functions, including dimethyl-hexa-decylamine (DMHDA), a volatile biosynthesized by Arthrobacter agilis UMCV2 that induces jasmonic acid (JA) signaling in Arabidopsis. Here, he found that the growth repressing effects of both DMHDA and JA are antagonized by kinetin and correlated with an inhibition of cytokinin-related ARR5::GUS and TCS::GFP expression in Arabidopsis primary roots. Moreover, we demonstrate that shoot supplementation of JA triggers JAZ1 expression both locally and systemically and represses cytokinin-dependent promoter activity in roots. A similar effect was observed after cotyledon wounding, in which an increase of JA-inducible LOX2:GUS expression represses root growth, which correlates with the loss of TCS::GFP detection at the very root tip. Our data demonstrate that the bacterial volatile DMHDA crosstalks with cytokinin signaling and reveals the downstream antagonistic interaction between JA and cytokinin in controlling root growth.

ALTERED MERISTEM PROGRAM 1 (AMP1) encodes a putative glutamate-carboxypeptidase important for plant growth and development. In this study, by comparing the growth of Arabidopsis wild-type, amp1-10 and amp1-13 mutants, and AMP1-GFP/OX2- and AMP1-GFP/OX7-overexpressing seedlings in vitro and in soil, we uncover the role of AMP1 in biomass accumulation in Arabidopsis. AMP1-overexpressing plants had longer primary roots and increased lateral root number and density than the WT, which correlated with improved root, shoot, and total biomass accumulation. AMP1-overexpressing seedlings had an enhanced rate of growth of primary roots, and accordingly, sucrose supplementation restored primary root growth and promoted lateral root formation in amp1 mutants, while reproductive development, fruit size, and seed content were also modified according to disruption or overexpression of AMP1. We further found that AMP1 plays an important role for stomatal development, guard cell functioning, and carbon assimilation. These data help explain the pleiotropic functions of AMP1 in both root and shoot system development, possibly acting in a sugar-dependent manner for regulation of root architecture, biomass accumulation, and seed production.