Physiological novelties for salinity tolerance created by transgressive effects and cryptic gene functions unlocked by alien introgression from Oryza rufipogon to Oryza sativa

The inherent complexity of adaptive mechanisms to salinity stress necessitates novel approaches to plant breeding. In rice, wide introgression is an approach that is yet to be fully exploited, especially from the not-so-distant species related to cultivars. We explored the genetic combining potential of the AA-genome wild species Oryza rufipogon, the closest progenitor of cultivated Oryza sativa ssp. japonica, to uncover physiological novelties for salinity tolerance created by transgressive effects. Comprehensive evaluation of a set of chromosome segment substitution lines (CSSL) for various physiometric traits revealed the occurrence of individuals transgressing the parental phenotypic range. This indicates that introgression of alien O. rufipogon genomic segments into O. sativa genomic background can alter the overall potential of the recipient by creating novel physiological attributes better than the donor or worse than the recipient. In-depth characterization of transgressive tolerant and transgressive sensitive CSSLs showed the occurrence of novel attributes in terms of energy balance and gas exchange that positively correlated with enhanced or reduced potential for salinity tolerance. Integrated morphological, physiological, biochemical, ionomic, genomic, and transcriptomic profiling revealed five genomic regions with QTL effects, and seven genes with putative eQTL effects that explain the occurrence of transgressive phenotypes. Genes with eQTL effects are associated with the regulation of cytokinin-mediated processes, MYB transcription factors, and transmembrane transport, that positively correlated with the maintenance of shoot biomass, regulation of stomatal conductance, and modulation of cellular homeostasis. The transgressive lines had non-parental expression patterns for eleven genes that originated from O. rufipogon. These genes gained new patterns of regulation (de-regulation effects) in the genomic background of O. sativa indicating the unleashing of cryptic functions through introgression. • Cryptic gene functions in O. rufipogon genome is unlocked by introgression into O. sativa genome. • Unlocked gene functions configured novel and transgressive salinity tolerance mechanisms. • Novel and non-parental adaptive traits are the outcomes of inter-species wide hybridization.