Changes in gene expression during germination reveal pea genotypes with either “quiescence” or “escape” mechanisms of waterlogging tolerance

Waterlogging causes germination failure in pea (Pisum sativum L.). Three genotypes (BARI Motorshuti‐3, Natore local‐2 [NL‐2], and Kaspa) contrasting in ability to germinate in waterlogged soil were exposed to different durations of waterlogging. Whole genome RNAseq was employed to capture differentially expressing genes. The ability to germinate in waterlogged soil was associated with testa colour and testa membrane integrity as confirmed by electrical conductivity measurements. Genotypes Kaspa and NL‐2 displayed different mechanisms of tolerance. In Kaspa, an energy conserving strategy was indicated by a strong upregulation of tyrosine protein kinsase and down regulation of linoleate 9S‐lipoxygenase 5, a fat metabolism gene. In contrast, a faster energy utilization strategy was suggested in NL‐2 by the marked upregulation of a subtilase family protein and peroxisomal adenine nucleotide carrier 2, a fat metabolizing gene. Waterlogging susceptibility in germinating seeds of genotype BARI Motorshuti‐3 was linked to upregulation of a kunitz‐type trypsin/protease inhibitor that blocks protein metabolism and may lead to excessive lipid metabolism and the membrane leakage associated with waterlogging damage. Pathway analyses based on gene ontologies showed seed storage protein metabolism as upregulated in tolerant genotypes and downregulated in the sensitive genotype. Understanding the tolerance mechanism provides a platform to breed for adaptation to waterlogging stress at germination in pea. Waterlogging is a major problem in cropping that is becoming more severe with increasing climatic variability. Three pea genotypes contrasting in ability to germinate in waterlogged soil were exposed to differing durations of waterlogging, and whole genome RNAseq was used to capture differentially expressing genes. We found testa membrane integrity following seed leakage strongly associated with waterlogging tolerance. Differential gene expression under waterlogging stress showed excessive lipid metabolism and membrane leakage in the sensitive genotype, whereas two tolerant genotypes displayed contrasting mechanisms of tolerance—quiescence or escape by regulating metabolism under stress.