Control of vein-forming, striped gene expression by auxin signaling

Abstract

Background Activation of gene expression in striped domains is a key building block of biological patterning, from the recursive formation of veins in plant leaves to that of ribs and vertebrae in our bodies. In animals, gene expression is activated in striped domains by the differential affinity of broadly expressed transcription factors for their target genes and the combinatorial interaction between such target genes. In plants, how gene expression is activated in striped domains is instead unknown. We address this question for the broadly expressed MONOPTEROS (MP) transcription factor and its target gene ARABIDOPSIS THALIANA HOMEOBOX FACTOR8 (ATHB8). Results We find that ATHB8 promotes vein formation and that such vein-forming function depends on both levels of ATHB8 expression and width of ATHB8 expression domains. We further find that ATHB8 expression is activated in striped domains by a combination of (1) activation of ATHB8 expression through binding of peak levels of MP to a low-affinity MP-binding site in the ATHB8 promoter and (2) repression of ATHB8 expression by MP target genes of the AUXIN/INDOLE-3-ACETIC-ACID-INDUCIBLE family. Conclusions Our findings suggest that a common regulatory logic controls activation of gene expression in striped domains in both plants and animals despite the independent evolution of their multicellularity.

Leaf vein patterning is regulated by the aperture of plasmodesmata intercellular channels

“…Our findings are consistent with the inability of plants with impaired ability to regulate PD aperture to restrict expression domains and maintain high expression levels of auxin response reporters in hypocotyl and root [ 24 , 86 , 87 ]. Our interpretation is consistent with high levels of auxin signaling at early stages of vein formation and low levels of auxin signaling at late stages of vein formation [ 48 , 88 ]. And mutual control of auxin signaling and PD aperture regulation is consistent with the finding that simultaneous inhibition of auxin signaling and of the ability to regulate PD aperture leads to vein patterning defects that are more severe than the addition of the defects induced by auxin signaling inhibition and those induced by impaired ability to regulate PD aperture.…”

“…Arrowheads temporally connect vein patterning stages with mature vein patterns. (A) In WT, veins are patterned by gradual restriction of auxin signaling domains [ 65 , 67 , 88 , 125 , 126 , 148 ], gradual restriction of auxin transport domains and polarization of auxin transport paths [ 5 , 37 , 38 , 56 , 65 – 67 , 126 , 148 ], and gradual reduction of PD permeability between incipient veins and surrounding nonvascular tissues. (B) Inhibition of auxin signaling leads to narrower domains of auxin transport [ 5 , 65 , 148 ] and promotes reduction of PD permeability between incipient veins and surrounding nonvascular tissues.…”

Genome-Wide Identification, Characterization, and Expression Analysis of the HD-Zip Gene Family in Lagerstroemia for Regulating Plant Height

“…By combining tissue-specific expression patterns with previous findings, several members of HD-Zip III and IV subfamilies were implicated in regulating Lagerstroemia plant height. For instance, two LinHDZs (LinHDZ24, and LinHDZ14) from the HD-Zip III subfamily were significantly upregulated in S_TS, with LinHDZ14 being homologous to ATHB8, reported to be regulated by AUX/IAA involved in auxin signaling [51]. Studies on Lagerstroemia plant architecture highlighted the significance of IAA and GA hormones in regulating plant height [31].…”

The Ins and Outs of Homeodomain-Leucine Zipper/Hormone Networks in the Regulation of Plant Development

“…It is worth mentioning that ATHB8, the fifth member of family III, has a distinct function in leaf development with respect to the other HD-ZIP III [ 49 ]. ATHB8 plays a role in promoting leaf vein formation downstream of auxin [ 148 , 149 , 150 ]. During leaf development, ATHB8 expression is activated in a single file of ground cells that will later elongate to become procambial cells, i.e., vascular precursors.…”