ARABIDOPSIS THALIANA HOMEOBOX GENE 1 controls plant architecture by locally restricting environmental responses

Abstract

Significance A major issue in plant biology is how plants are shaped by the interaction between internal genetic programs—for example, those that form boundaries between leaves and the stem—and environmental signals such as light quality, which induces stem elongation in shade conditions. In many plant species, stem growth is suppressed during the vegetative phase, resulting in a compact whorl of leaves called a rosette. We show that the rosette habit of Arabidopsis is conferred by a gene involved in organ boundary formation, together with gibberellin hormone signaling, both of which antagonize genes that mediate organ growth in response to light. In this way, a common type of plant architecture results from localized inhibition of environmentally responsive growth. The diversity and environmental plasticity of plant growth results from variations of repetitive modules, such as the basic shoot units made of a leaf, axillary bud, and internode. Internode elongation is regulated both developmentally and in response to environmental conditions, such as light quality, but the integration of internal and environmental signals is poorly understood. Here, we show that the compressed rosette growth habit of Arabidopsis is maintained by the convergent activities of the organ boundary gene ARABIDOPSIS THALIANA HOMEOBOX GENE 1 (ATH1) and of the gibberellin-signaling DELLA genes. Combined loss of ATH1 and DELLA function activated stem development during the vegetative phase and changed the growth habit from rosette to caulescent. Chromatin immunoprecipitation high-throughput sequencing and genetic analysis indicated that ATH1 and the DELLA gene REPRESSOR OF GA1-3 (RGA) converge on the regulation of light responses, including the PHYTOCHROME INTERACTING FACTORS (PIF) pathway, and showed that the ATH1 input is mediated in part by direct activation of BLADE ON PETIOLE (BOP1 and BOP2) genes, whose products destabilize PIF proteins. We conclude that an organ-patterning gene converges with hormone signaling to spatially restrict environmental responses and establish a widespread type of plant architecture.