A bHLH Complex Controls Embryonic Vascular Tissue Establishment and Indeterminate Growth in Arabidopsis

Abstract

Plants have a remarkable potential for sustained (indeterminate) postembryonic growth. Following their specification in the early embryo, tissue-specific precursor cells first establish tissues and later maintain them postembryonically. The mechanisms underlying these processes are largely unknown. Here we define local control of oriented, periclinal cell division as the mechanism underlying both the establishment and maintenance of vascular tissue. We identify an auxin-regulated basic helix-loop-helix (bHLH) transcription factor dimer as a critical regulator of vascular development. Due to a loss of periclinal divisions, vascular tissue gradually disappears in bHLH-deficient mutants; conversely, ectopic expression is sufficient for triggering periclinal divisions. We show that this dimer operates independently of tissue identity but is restricted to a small vascular domain by integrating overlapping transcription patterns of the interacting bHLH proteins. Our work reveals a common mechanism for tissue establishment and indeterminate vascular development and provides a conceptual framework for developmental control of local cell divisions.

Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo

“…Nonetheless, we have demonstrated the role of several MP target genes in hypophysis specification (17) and vascular tissue establishment (18,19) through transcriptome profiling of mp seedlings, as well as seedlings in which ARF activity was inhibited by an inducible version of the dominant mutant ARF inhibitor BODENLOS/IAA12 (BDL) (20,21). The BDL transcriptional repressor is normally degraded in response to auxin, resulting in ARF-dependent gene expression (22), but as the bdl mutation prevents degradation (21), this…”

“…We thus locally inhibited MP activity in the putative first vascular and ground tissue cells via GAL4-UAS-based (23) expression of a mutant bdl protein to identify embryonic MP target genes. MP controls the stereotypic division of the first vascular cells and hypophyseal cell in the globular-stage embryo (15,18). We crossed UAS::bdl plants with Q0990 plants (Q0990>>bdl) and observed that globular-stage embryos showed vascular and hypophysis division defects after 3 d (Fig.…”

“…We examined early mp mutant embryos that were recognizable through aberrant hypophysis division and frequent aberrant division of the first vascular cells (Fig. 1 H and I) (18). Remarkably, although this aspect of the mp mutant phenotype has remained unnoticed despite ongoing investigation of the mp mutant since its isolation 25 y ago, we observed abnormally oriented division planes in the first ground tissue cells in ∼50% of mp mutant embryos, in two independent mp alleles (46.9% division defects in at least one of the two cells in median view, n = 49 embryos for mpB4149; 57.1% division defects, n = 49 for mpS319; 0% division defects in Col-0, n = 57; 1.9% defects in Utrecht ecotype, n = 53; mpB4149 is in Utrecht background).…”

Molecular genetic framework for protophloem formation

“…Mutant analyses in Arabidopsis have identified various genes involved in the formation of vascular tissues (1,3,(5)(6)(7)(8)(9). In addition to upstream regulators required for overall vascular morphogenesis, these screens have also identified factors that are specifically involved in xylem or phloem development.…”

Theoretical approaches to understanding root vascular patterning: a consensus between recent models

“…Amongst other targets, MP promotes the expression of a basic helix-loop-helix transcription factor, TARGET OF MONOPTEROS 5 (TMO5) (Schlereth et al, 2010). Together with its homologs, TMO5 forms heterodimers with the LONESOME HIGHWAY (LHW) group of helix-loop-helix transcription factors to determine the frequency and orientation of cell divisions within the vascular cylinder (De Rybel et al, 2013;Katayama et al, 2016).…”