Pea (Pisum sativum L.), like most legumes, forms mutualistic symbioses with nodule bacteria and arbuscular mycorrhizal (AM) fungi. The positive effect of inoculation is partially determined by the plant genotype; thus, pea varieties with high and low symbiotic responsivity have been described, but the molecular genetic basis of this trait remains unknown. Here, we compare the symbiotically responsive breeding line ‘Triumph’ of grain pea with its parental cultivars ‘Vendevil’ (a donor of high symbiotic responsivity) and ‘Classic’ (a donor of agriculturally valuable traits) using genome and transcriptome sequencing. We show that ‘Triumph’ inherited one-fourth of its genome from ‘Vendevil’, including the genes related to AM and nodule formation, and reveal that under combined inoculation with nodule bacteria and AM fungi, ‘Triumph’ and ‘Vendevil’, in contrast to ‘Classic’, demonstrate similar up-regulation of the genes related to solute transport, hormonal regulation and flavonoid biosynthesis in their roots. We also identify the gene PsGLP2, whose expression pattern distinguishing ‘Triumph’ and ‘Vendevil’ from ‘Classic’ correlates with difference within the promoter region sequence, making it a promising marker for the symbiotic responsivity trait. The results of this study may be helpful for future molecular breeding programs aimed at creation of symbiotically responsive cultivars of pea.

Pea (Pisum sativum L.), like most legumes, forms mutualistic symbioses with nodule bacteria and arbuscular mycorrhizal (AM) fungi. The positive effect of inoculation is partially determined by the plant genotype, thus, pea varieties with high and low symbiotic responsivity have been described, but the molecular genetic basis of this trait remains unknown. Here, we compare the symbiotically responsive breeding line ‘Triumph’ of grain pea with its parental cultivars ‘Vendevil’ (a donor of high symbiotic responsivity) and ‘Classic’ (a donor of agriculturally valuable traits) using genome and transcriptome sequencing. We show that ‘Triumph’ inherited one-fourth of its genome from ‘Vendevil’, including the genes related to AM and nodule formation, and reveal that under combined inoculation with nodule bacteria and AM fungi, ‘Triumph’ and ‘Vendevil’, in contrast to ‘Classic’, demonstrate similar up-regulation of the genes related to solute transport, hormonal regulation and flavonoid biosynthesis in their roots. We also identify the gene PsGLP2, whose expression pattern distinguishing ‘Triumph’ and ‘Vendevil’ from ‘Classic’ correlates with difference within the promoter region sequence, making it a promising marker for the symbiotic responsivity trait. The results of the study may be helpful for future molecular breeding programs aimed at creation of symbiotically responsive cultivars of pea.

In pea (Pisum sativum L.), alleles of the Sym2 gene determine the specificity of the interaction with nodule bacteria (rhizobia). The Sym2^A allele present in landraces from Afghanistan provides higher selectiveness toward rhizobia than the Sym2^E allele present in European cultivars. Rhizobial strains possessing the nodX gene can interact with both Sym2^A and Sym2^E peas, while strains lacking nodX can interact only with Sym2^E peas. Here, we studied the previously obtained introgression line A33.18 bearing Sym2^A in a homozygous state in the genome of the European pea cultivar ‘Rondo’. A33.18 has proved its high selectiveness in pot experiments. Genome sequencing has shown that A33.18 possesses an 18.2 Mb region inherited from Afghanistan pea with 63 genes, including 5 receptor kinase genes, among which was the Sym2 candidate gene LykX. In a field experiment, under inoculation with the nodX⁺ strain TOM, over 95% of nodules of A33.18 contained TOM, as opposed to less than 8% of nodules containing TOM in the parental European cultivar ‘Rondo’. Thus, introgression of Sym2^A enabled peas to interact specifically with the nodX⁺ strain, favoring the formation of nodules by the strain from the inoculum and protecting peas from the indigenous soil microbiota.