Genetic Architecture of Heterophylly: Single and Multi-Leaf Genome-Wide Association Mapping in Populus euphratica

Abstract

Heterophylly is an adaptive strategy used by some plants in response to environmental changes. Due to the lack of representative plants with typical heteromorphic leaves, little is known about the genetic architecture of heterophylly in plants and the genes underlying its control. Here, we investigated the genetic characteristics underlying changes in leaf shape based on the model species, Populus euphratica, which exhibits typical heterophylly. A set of 401,571 single-nucleotide polymorphisms (SNPs) derived from whole-genome sequencing of 860 genotypes were associated with nine leaf traits, which were related to descriptive and shape data using single- and multi-leaf genome-wide association studies (GWAS). Multi-leaf GWAS allows for a more comprehensive understanding of the genetic architecture of heterophylly by considering multiple leaves simultaneously. The single-leaf GWAS detected 140 significant SNPs, whereas the multi-leaf GWAS detected 200 SNP-trait associations. Markers were found across 19 chromosomes, and 21 unique genes were implicated in traits and serve as potential targets for selection. Our results provide novel insights into the genomic architecture of heterophylly, and provide candidate genes for breeding or engineering P. euphratica. Our observations also improve understanding of the intrinsic mechanisms of plant growth, evolution, and adaptation in response to climate change.

Integrating genome-wide association and transcriptome analysis to provide molecular insights into heterophylly and eco-adaptability in woody plants

“…It should be noted that our study also identified some other key genes through GWAS and WGCNA analyses, such as cytochrome P450 ( Bp07g0752 , Bp07g0237 ), WD repeat-containing protein ( Bp02g0499 ), UDP-glycosyltransferase ( Bp08g0037 ), and serine/threonine-protein kinase ( Bp05g0658 ), which might also be involved in the regulation of heterophylly in woody plants. Consistent with this view, the previous GWAS analysis in P. euphratica also identified significant genes associated with heterophylly, which encoded WD repeat-containing protein, serine/threonine-protein kinase [ 23 ], and cytochrome P450 [ 22 ]. Moreover, this study identified a series of DEGs encoding KNOX, TCP, CUC, BEL, and Dof transcription factors, which are also important for leaf development and heterophylly of plants.…”

“…To adapt to the changeable environment, plants have formed a variety of adaptive strategies; altering leaf morphology is one of the important adaptation mechanisms for heterophyllous plants [ 27 , 28 ]. Although heterophylly has been the subject of a preliminary study in aquatic and amphibian plants [ 6 , 10 ], the genetic basis for eco-adaptability of heterophyllous leaves is still unclear in terrestrial woody plants, and the relevant studies were mainly carried out in Populus euphratica [ 22 , 24 , 29 ]. To further clarify the mechanisms underlying heterophylly in woody plant species, we systematically and comprehensively evaluated the variation of heterophyllous leaves in a natural population of paper mulberry, which exhibits significant heterophylly and eco-adaptability [ 30 ].…”

“…Recently, with the rise of sequencing technology, GWAS analysis, transcriptome analysis, and proteome techniques have also been applied to elucidate the genetic mechanism of heterophylly in plants. For example, GWAS analysis has detected 340 significant single-nucleotide polymorphisms (SNPs) and 21 unique genes associated with heterophylly, including the transcription factor MYB, the auxin response factor 19, and cytochrome P450 [ 22 ]. Another GWAS analysis in P. euphratica identified a series of candidate genes participating in auxin, shape, and stress resistance, and the results suggest that auxin response factor17-like ( ARF17 ) is involved in the regulation of heterophylly [ 23 ].…”