Contributions of Adaptive Plant Architecture to Transgressive Salinity Tolerance in Recombinant Inbred Lines of Rice: Molecular Mechanisms Based on Transcriptional Networks

Abstract

Genetic novelties are important nucleators of adaptive speciation. Transgressive segregation is a major mechanism that creates genetic novelties with morphological and developmental attributes that confer adaptive advantages in certain environments. This study examined the morpho-developmental and physiological profiles of recombinant inbred lines (RILs) from the salt-sensitive IR29 and salt-tolerant Pokkali rice, representing the total range of salt tolerance including the outliers at both ends of the spectrum. Morpho-developmental and physiological profiles were integrated with a hypothesisdriven interrogation of mRNA and miRNA transcriptomes to uncover the critical genetic networks that have been rewired for novel adaptive architecture. The transgressive super-tolerant FL510 had a characteristic small tiller angle and wider, more erect, sturdier, and darker green leaves. This unique morphology resulted in lower transpiration rate, which also conferred a special ability to retain water more efficiently for osmotic avoidance. The unique ability for water retention conferred by such adaptive morphology appeared to enhance the efficacy of defenses mediated by Na + exclusion mechanism (SalTol-effects) inherited from Pokkali. The super-tolerant FL510 and super-sensitive FL499 had the smallest proportions of differentially expressed genes with little overlaps. Genes that were steadily upregulated in FL510 comprised a putative cytokininregulated genetic network that appeared to maintain robust growth under salt stress through well-orchestrated cell wall biogenesis and cell expansion, likely through major regulatory (OsRR23, OsHK5) and biosynthetic (OsIPT9) genes in the cytokinin signaling pathway. Meanwhile, a constitutively expressed cluster in FL510 prominently featured two transcription factors (OsIBH1, TAC3) that control tiller angle and growth habit through the brassinosteroid signaling pathway. Both the putative cytokinin-mediated and brassinosteroid-mediated clusters appeared to function as highly coordinated network synergies in FL510. In contrast, both networks appeared to be sub-optimal and inferior in the other RILs and parents as they were disjointed and highly fragmented. Transgressively expressed miRNAs (miR169, miR397, miR827) were also identified as

DECUSSATEnetwork with flowering genes explains the variable effects ofqDTY12.1to rice yield under drought across genetic backgrounds

“…A similar phenomenon has been reported on SalTol for salinity tolerance in different rice cultivars, when introgression of the QTL alone did not necessarily lead to the expected phenotypic effects (Han et al., 2020; Pabuayon et al., 2021). Inconsistencies are caused by negative or positive epistatic interactions between the QTL genes and other genes in the genetic background that could either enhance or drag the QTL effects (de los Reyes, 2019; Pabuayon et al., 2020). We further illuminated this enigma by integrating the concept of the Omnigenic theory (Boyle et al., 2017) and by using transgressive mechanisms to support our conceptual framework (de los Reyes, 2019; Pabuayon et al., 2021; Pabuayon et al., 2020).…”

“…Inconsistencies are caused by negative or positive epistatic interactions between the QTL genes and other genes in the genetic background that could either enhance or drag the QTL effects (de los Reyes, 2019; Pabuayon et al., 2020). We further illuminated this enigma by integrating the concept of the Omnigenic theory (Boyle et al., 2017) and by using transgressive mechanisms to support our conceptual framework (de los Reyes, 2019; Pabuayon et al., 2021; Pabuayon et al., 2020).…”

“…It was postulated that nonparental traits created by genetic recombination are due to genetic coupling–uncoupling and network rewiring effects. Rewired genetic networks are caused by large assemblages of synergistic or antagonistic alleles that get coupled or uncoupled during multiple rounds of recombination (de los Reyes, 2019; Pabuayon et al., 2021; Pabuayon et al., 2020). In the context of the Omnigenic theory, the few core genes/alleles with major effects on phenotypic variance could either be coupled or uncoupled with numerous compatible or incompatible peripheral genes/alleles with minute but additive effects on the phenotypic variance (Boyle et al., 2017).…”

“…With this reality in mind, innovative and holistic paradigms in plant breeding become critical to the development of the next generation of crop cultivars that can absorb this conglomeration of ecological factors while minimizing penalties to yield. The creation of novel ideotypes with resilience to drought‐prone environments, for example, holds great promise for maximizing yield under suboptimal conditions (de los Reyes, 2019; Pabuayon et al., 2020).…”

Yield maintenance under drought is orchestrated by theqDTY12.1-encodedDECUSSATEgene of rice through a network with other flowering-associated genes across the genetic background

“…With this reality in mind, innovative and holistic paradigms in plant breeding will be critical to the development of the next generation of crop cultivars that can absorb this conglomeration of ecological factors while minimizing penalties to yield. The creation of new ideotypes with novel mechanisms that confer resilience to drought-prone environments for example, holds great promise for establishing an effective means for maximizing yield under sub-optimal conditions [7,8].…”