Coping with stress: Transcriptional regulators linking cell wall integrity maintenance with primary-wall metabolism in Arabidopsis thaliana

Abstract

Cell wall damage (CWD) and hyperosmotic stress elicit both distinct and overlapping transcriptional programs in plants. Responses to these stresses involve cell wall integrity (CWI) maintenance, which is mediated by receptor-like kinases such as THESEUS1 (THE1), yet the downstream regulators linking early signalling to primary cell-wall metabolism and stress-induced phytohormone biosynthesis remain poorly defined. We induced CWD and hyperosmotic stress in wild type and the1 mutant alleles with isoxaben (ISX) and sorbitol, and analysed the gene expression of treated seedlings by RNA-seq. From these data, we focused on 15 transcriptional regulators whose expression was responsive to treatments and showed dependency on THE1 activity. Following up, we performed various functional analyses in mutant lines of these candidates and identified transcription factors that influence primary cell-wall metabolism, growth, transcriptional control of cellulose production, resistance to CWD and hyperosmotic stress, as well as phytohormone and lignin biosynthesis. Our results identify JMJ17, bHLH, and CBP60A as essential transcriptional regulators involved in responses to CWD and hyperosmotic stress, and they provide a starting point for dissecting the transcriptional network that regulates CWI maintenance and primary cell wall metabolism. This study sheds light on a previously unknown signalling network that regulates primary cell wall synthesis in control and stress conditions, providing a basis for more resilient crop plant breeding in the future. Significance StatementPlants provide food and materials used by society, and their productivity depends on maintaining cell wall integrity (CWI) during growth, development, and environmental stress. The CWI maintenance mechanism, involving receptor-like kinases such as THESEUS1 (THE1), has been extensively investigated, yet the transcriptional regulators involved in primary wall metabolism and stress-induced phytohormone production remain unknown. Here, we integrate transcriptomics with functional genetic and physiological assays to identify transcription factors acting in a THE1-dependent/independent manner. These regulators link CWI, hyperosmotic stress, and cell wall damage to primary wall metabolism, lignification, phytohormone production, and root growth. Our findings reveal elements of the transcriptional network that coordinate CWI and primary cell wall formation with adaptive responses, generating insights to enhance crop stress resilience.