Salinity tolerance in wild rice relatives : expanding the genetic pool for cultivated rice improvement

Salinity stress affects global food-producing areas by limiting both crop growth and yield. Finding suitable donors of genes and traits for salinity tolerance has become a major bottleneck in breeding for salinity tolerant crops. Attempts to develop salinity-tolerant rice varieties have had limited success due to the complexity of the salinity tolerance trait, high variation in stress response and lack of available donors for candidate genes for cultivated rice. Wild relatives of rice have long been known to have superior performance in harsh environments, such as salinity. Identifying the key traits involved in differential salinity tolerance between wild and cultivated rice and understanding how it evolve within species could highlight its potential use to provide breeders with novel resources in producing salinity tolerant varieties. In this study, we evaluated the physiological and molecular adaptive mechanism of 8 wild Oryza species with representatives in primary, secondary and tertiary gene pool alongside cultivated salinity check cultivars Pokalli (tolerant) and IR29 and Koshihikari (sensitive) under control and salinity stress condition. We surveyed the evolution of salinity tolerant gene family responsible for differential tolerance amongst wild and cultivated Oryza species and performed transcriptional studies on how the presence of distinct leaf anatomical trait present in halophilic wild rice Oryza coarctata play a functional significance to its superior tolerance to salinity stress. Major findings are as follows: (1) Wild rice species showed superior overall growth performance with the least reduction in whole-plant growth, leaf tissue damage, photosynthetic capacity and yield most notably with halophilic wild rice Oryza coarctata where no significant changes observed under salinity treatment. (2) In contrast with cultivated rice, confocal imaging measuring leaf Na⁺ accumulation in leaf mesophyll cells and ion content quantification demonstrates that wild rice exhibits superior tissue tolerance maintaining stable physiological traits while accumulating Na⁺ ions in the leaf. (3) Differential gene expression patterns of known salt tolerant genes involved in ion homeostasis was observed and the expression of NHX1 and SOS1/NHX7 exhibited significant correlation with salt tolerance among cultivated and wild rice species. 4) Phylogenetic analysis of NHX1 revealed that tissue tolerance had evolved in Oryza genus which genetic trait diversity was probably reduced in the course of domestication affecting the current salinity tolerance in cultivated rice. (5) The presence of unique functional leaf architecture such as larger and higher number of bundle sheath cells in O. coarctata which also not found in other Oryza species confers cell-type-specific ion regulation and transcriptional response to salinity stress. We conclude amongst all wild relatives the naturally occurring allotetraploids in secondary and tertiary gene pool such as O. coarctata, O. latifolia and O. alta and the inclusion of tissue tolerance in salinity tolerance screening can be targeted in future genetic programs to develop salinity tolerant cultivated rice.