Abstract
SummaryPhotosynthesis is a key reaction that ultimately generates the carbohydrates needed to form woody tissues in trees. However, the genetic regulatory network of protein‐encoding genes (PEGs) and regulatory noncoding RNAs (ncRNAs), including microRNAs (miRNAs) and long noncoding RNAs (lncRNAs), underlying the photosynthetic pathway is unknown. Here, we integrated data from coexpression analysis, association studies (additive, dominance and epistasis), and expression quantitative trait nucleotide (eQTN) mapping to dissect the causal variants and genetic interaction network underlying photosynthesis in Populus. We initially used 30 PEGs, 6 miRNAs and 12 lncRNAs to construct a coexpression network based on the tissue‐specific gene expression profiles of 15 Populus samples. Then, we performed association studies using a natural population of 435 unrelated Populus tomentosa individuals, and identified 72 significant associations (P ≤ 0.001, q ≤ 0.05) with diverse additive and dominance patterns underlying photosynthesis‐related traits. Analysis of epistasis and eQTNs revealed that the complex genetic interactions in the coexpression network contribute to phenotypes at various levels. Finally, we demonstrated that heterologously expressing the most highly linked gene (PtoPsbX1) in this network significantly improved photosynthesis in Arabidopsis thaliana, pointing to the functional role of PtoPsbX1 in the photosynthetic pathway. This study provides an integrated strategy for dissecting a complex genetic interaction network, which should accelerate marker‐assisted breeding efforts to genetically improve woody plants.
Highlights
Photosynthesis is a crucial process that determines the rate of carbon dioxide fixation in green plants and the levels of carbohydrates that are used to produce woody tissues in trees (Schaedle 1975; Niinemets 2014)
To search for gene transcripts involved in the core photosynthetic pathway, we investigated the overall transcriptional activity in the leaves of 1-year-old P. tomentosa clone ‘1316’ via RNA-seq and detected 21 366 expressed protein-encoding genes (PEGs) in leaves
We performed Gene Ontology (GO) enrichment analysis and determined that 94 PEGs clustered into three GO terms related to the biological process of photosynthesis (GO: 0009765, GO: 0015979 and GO: 0019684) (Table S1), suggesting that these PEGs are involved in the photosynthetic pathway
Summary
Photosynthesis is a crucial process that determines the rate of carbon dioxide fixation in green plants and the levels of carbohydrates that are used to produce woody tissues in trees (Schaedle 1975; Niinemets 2014). Improving our understanding of the molecular mechanism of photosynthesis is essential for increasing plant growth and biomass accumulation. Recent studies have shown that the genetic modification of genes involved in the photosynthetic pathway can alter the maximum photosynthetic efficiency and biomass of plants (Heyneke & Fernie 2018). Several transcriptomic and proteomic studies have analysed the interplay between photosynthesis and biotic and abiotic stress tolerance in perennial trees with the aim of uncovering the regulatory mechanism of stress-induced suppression of photosynthesis (Bernacki et al, 2018; Chen 2018). The roles of several stress response genes in regulating photosynthesis have been identified via transgenic analysis in perennial trees. Several studies have demonstrated the important roles of various individual genes in the photosynthetic pathway, the genetic architecture of the targeted photosynthesis-related traits remains unknown, especially the magnitude of the genetic effects of causal genes and alleles, as well as the allelic interactions among genes involved in the photosynthetic pathway
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