Novel and Transgressive Salinity Tolerance in Recombinant Inbred Lines of Rice Created by Physiological Coupling-Uncoupling and Network Rewiring Effects

Abstract

The phenomenon of transgressive segregation, where a small minority of recombinants are outliers relative to the range of parental phenotypes, is commonly observed in plant breeding populations. While this phenomenon has been attributed to complementation and epistatic effects, the physiological and developmental synergism involved have not been fully illuminated by the QTL mapping approach alone, especially for stress-adaptive traits involving highly complex interactions. By systems-level profiling of the IR29 × Pokkali recombinant inbred population of rice, we addressed the hypothesis that novel salinity tolerance phenotypes are created by reconfigured physiological networks due to positive or negative coupling-uncoupling of developmental and physiological attributes of each parent. Real-time growth and 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. 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 synergism uncovered by the phenomics approach in this study supports the modern views of the Omnigenic Theory, emphasizing the synergy or lack thereof between core and peripheral components. This study also supports a breeding paradigm rooted on genomic modeling from multi-dimensional genetic, physiological, and phenotypic profiles to create novel adaptive traits for new crop varieties of the 21st century.

Description
Copyright © 2021 Pabuayon, Kitazumi, Cushman, Singh, Gregorio, Dhatt, Zabet-Moghaddam, Walia and de los Reyes. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Keywords
Genetic Novelty, Genetic Network Rewiring, Salinity Stress, Transgressive Segregation, Physiological and Biochemical Synergy, Omnigenic Theory
Citation
Pabuayon ICM, Kitazumi A, Cushman KR, Singh RK, Gregorio GB, Dhatt B, Zabet-Moghaddam M, Walia H and de los Reyes BG (2021) Novel and Transgressive Salinity Tolerance in Recombinant Inbred Lines of Rice Created by Physiological Coupling-Uncoupling and Network Rewiring Effects. Front. Plant Sci. 12:615277. https://doi.org/10.3389/fpls.2021.615277
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