Transgressive segregation for salt tolerance in rice due to physiological coupling and uncoupling and genetic network rewiring

Transgressive segregation is common in plant breeding populations, where a small minority of recombinants are outliers relative to parental phenotypes. While this phenomenon has been attributed to complementation and epistatic effects, the physiological, biochemical, and molecular bases have not been fully illuminated. By systems-level scrutiny of the IR29 x Pokkali recombinant inbred population of rice, we addressed the hypothesis that novel salt tolerance phenotypes are created by positive or negative coupling or uncoupling effects and novel regulatory networks. Hyperspectral profiling distinguished the transgressive individuals in terms of stress penalty to growth. Non-parental network signatures that led to either optimal or non-optimal integration of developmental with stress-related mechanisms were evident at the macro-physiological, biochemical, metabolic, and transcriptomic levels. The large positive net gain in super-tolerant progeny was due to ideal complementation of beneficial traits, while shedding antagonistic traits. Super-sensitivity was explained by the stacking of multiple antagonistic traits and loss of major beneficial traits. The mechanisms elucidated in this study are consistent with the Omnigenic Theory, emphasizing the synergy or lack thereof between core and peripheral components. This study supports a breeding paradigm based on genomic modeling to create the novel adaptive phenotypes for the crops of the 21st century.