Above and belowground phenotypic response to exogenous auxin across Arabidopsis thaliana mutants and natural accessions varies from seedling to reproductive maturity

Abstract

Background Plant hormones influence phenology, development, and function of above and belowground plant structures. In seedlings, auxin influences the initiation and development of lateral roots and root systems. How auxin-related genes influence root initiation at early life stages has been investigated from numerous perspectives. There is a gap in our understanding of how these genes influence root size through the life cycle and in mature plants. Across development, the influence of a particular gene on plant phenotypes is partly regulated by the addition of a poly-A tail to mRNA transcripts via alternative polyadenylation (APA). Auxin related genes have documented variation in APA, with auxin itself contributing to APA site switches. Studies of the influence of exogenous auxin on natural plant accessions and mutants of auxin pathway gene families exhibiting variation in APA are required for a more complete understanding of genotype by development by hormone interactions in whole plant and fitness traits. Methods We studied Arabidopsis thaliana homozygous mutant lines with inserts in auxin-related genes previously identified to exhibit variation in number of APA sites. Our growth chamber experiment included wildtype Col-0 controls, mutant lines, and natural accession phytometers. We applied exogenous auxin through the life cycle. We quantified belowground and aboveground phenotypes in 14 day old, 21 day old seedlings and plants at reproductive maturity. We contrasted root, rosette and flowering phenotypes across wildtype, auxin mutant, and natural accession lines, APA groups, hormone treatments, and life stages using general linear models. Results The root systems and rosettes of mutant lines in auxin related genes varied in response to auxin applications across life stages and varied between genotypes within life stages. In seedlings, exposure to auxin decreased size, but increased lateral root density, whereas at reproductive maturity, plants displayed greater aboveground mass and total root length. These differences may in part be due to a shift which delayed the reproductive stage when plants were treated with auxin. Root traits of auxin related mutants depended on the number of APA sites of mutant genes and the plant’s developmental stage. Mutants with inserts in genes with many APA sites exhibited lower early seedling belowground biomass than those with few APA sites but only when exposed to exogenous auxin. As we observed different responses to exogenous auxin across the life cycle, we advocate for further studies of belowground traits and hormones at reproductive maturity. Studying phenotypic variation of genotypes across life stages and hormone environments will uncover additional shared patterns across traits, assisting efforts to potentially reach breeding targets and enhance our understanding of variation of genotypes in natural systems.