Genome-wide association studies reveal the coordinated regulatory networks underlying photosynthesis and wood formation in Populus.

Photosynthesis and wood formation underlie the ability of trees to provide renewable resources and perform ecosystem services; however, the genetic basis and regulatory pathways coordinating these two linked processes remain unclear. Here, we used a systems genetics strategy, integrating genome-wide association study, transcriptomic analyses, and transgenic experiments, to investigate the genetic architecture of photosynthesis and wood properties among 435 unrelated individuals of Populus tomentosa and unravel the coordinated regulatory networks causative of two trait categories. We totally detected 222 significant single-nucleotide polymorphisms, annotated to 177 candidate genes, for 10 traits of photosynthesis and wood properties. Epistasis uncovered 74 epistatic interactions for phenotypes. Strikingly, we deciphered the coordinated regulation patterns of pleiotropic genes underlying phenotypic variations for two trait categories. Furthermore, expression quantitative trait nucleotide mapping and coexpression analysis were integrated to unravel the potential transcriptional regulatory networks of candidate genes coordinating photosynthesis and wood properties. Finally, we heterologously expressed two pleiotropic genes, PtoMYB62 and PtoMYB80, in Arabidopsis thaliana, and demonstrated that they coordinate regulatory networks balancing photosynthesis and stem secondary cell wall components, respectively. Our study provides insight into the regulatory mechanisms coordinating photosynthesis and wood formation in poplar, which will accelerate the genetic breeding in trees via molecular design.