Genetic dissection of the gene coexpression network underlying photosynthesis in Populus

Abstract

Summary Photosynthesis 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.

Association Study and Mendelian Randomization Analysis Reveal Effects of the Genetic Interaction Between PtoMIR403b and PtoGT31B-1 on Wood Formation in Populus tomentosa

“…Several SNPs were predicted to affect the secondary structure of pre-miRNA. An SNP in the mature region of PtoMIR6466 that alters the stemloop structure and was associated with photosynthetic traits (Xiao et al, 2020). Herein, we identified five SNPs in PtoMIR403b significantly associated with wood characteristic traits, suggesting a role for PtomiR403b in wood formation (Figure 2).…”

“…Epistasis is an interaction effect among multiple variants or genes that contribute to the same traits, and its analysis can reveal genetic interactions between two SNPs or genes underlying complex traits. We previously used the epistasis association study to construct a genetic interaction network for photosynthetic traits and revealed the allelic combinations among non-coding RNAs and protein-coding gene, suggesting the power of epistatic effects to illustrate the genetic interaction between miRNA and its target genes (Xiao et al, 2020). We identified 36 SNP-SNP pairs representing the interactions between PtoMIR403b and PtoGT31B-1 and clarified how these interactions contribute to wood characteristic traits (Figure 3), revealing that PtoMIR403b and PtoGT31B-1 interact and are involved the same regulatory pathway.…”

Genetic Effects and Expression Patterns of the Nitrate Transporter (NRT) Gene Family in Populus tomentosa

“…As described in a previous manuscript, a 10-year-old association population of 435 unrelated individuals was vegetatively propagated in Guanxian County, Shandong Province, China (36° 23′N, 115° 47′E) in 2009, from root segments, using a random complete block design of three blocks ( Xiao et al, 2020 ). The sampled population was randomly selected from 1047 individuals from natural P. tomentosa populations, representing almost the entire natural distribution of P. tomentosa (30-40° N, 105-125° E), which can be divided into three climatic regions ( Zhang et al, 2010 ).…”

Genetic Architecture Underlying the Metabolites of Chlorogenic Acid Biosynthesis in Populus tomentosa

“…The methods for genome resequencing and genotyping have been described by Xiao et al [ 50 ]. Briefly, the total genomic DNA was extracted from fresh mature leaves of 300 unrelated individuals using the DNeasy plant Mini Kit (Qiagen, Shanghai, China), and a re-sequencing library was constructed according to the sample preparation instructions (Illumina, San Diego, CA, USA).…”