Integrated phenotyping, genomics, and transcriptomics reveal a constitutive drought-responsive regulatory state associated with drought adaptation in wild rice

Abstract

Improving drought tolerance is crucial for sustainable crop production under climate change. Identifying drought-adaptive variation in diverse genetic resources, including crop wild relatives, requires accurate and temporally resolved assessment of plant responses to water deficit. Here, we developed an indoor, unmanned phenotyping platform that can noninvasively and automatically collect temporal data on plant responses to drought stress. Using this platform, we quantified temporal drought responses in four rice cultivars and five wild rice relatives and integrated these phenotypes with chromosome-scale genome assemblies, gene annotations, and time-course transcriptomes. This integrated phenotyping, genomics, and transcriptomics identified a wild rice accession that maintained shoot growth, leaf temperature, and gene expression more stably under drought stress and exhibited a distinctive constitutive drought-responsive transcriptional state. This state included elevated basal expression of several drought-responsive genes, including ABSCISIC ACID RESPONSIVE ELEMENT-BINDING FACTOR 1 (ABF1), a known regulator of ABA-mediated drought responses. Validation using transgenic and introgression lines suggested that low-level constitutive ABF1 expression, as a component of this drought-responsive regulatory state, can improve drought performance without obvious growth penalties. These findings demonstrate the utility of automated temporal phenotyping combined with accession-specific genomic and transcriptomic resources for uncovering drought-adaptive variation in wild rice, and provide a framework for exploiting natural regulatory variation to improve drought resilience in cultivated rice.