Wild rice research: Advancing plant science and food security

Abstract

Rice was domesticated in Asia (Oryza sativa) and Africa (Oryza glaberrima) from Oryza rufipogon and Oryza bathii, respectively. The Oryza genus has a pantropical distribution. The genetic diversity in Oryza provides an extensive gene pool to adapt rice to climate change and address future food security. The primary gene pool of domesticated rice includes species that are readily accessible for rice breeding due to ease of crossing, while more distant species are also sources of useful genes that can be recovered with greater difficulty (Figure 1). Advances in genomics and gene editing provide a path for use of this wider diversity. Studies of Oryza species also offer potential insights into rice biology that may be critical for ongoing rice food security. Wild rice provides a much larger gene pool than that available within domesticated rice. Oryza includes more than 20 wild species (Henry and Mondal, 2018Henry R.J. Mondal T.K. The Wild Oryza Genomes. Compendium of Plant Genomes.1st edn. Springer International Publishing, 2018Google Scholar). However, the gene pool provided by the whole Oryza genus (Figure 1) has had very limited use in rice improvement and even the diversity in the primary gene pool provided by the AA genome species has been poorly utilized. For example, analysis of the chloroplast genomes has shown that only two functionally distinct genotypes are present in domesticated rice, while wild AA genome rices have a great diversity of chloroplast genomes (Moner et al., 2020Moner A.M. Furtado A. Henry R.J. Two divergent chloroplast genome sequence clades captured in the domesticated rice gene pool may have significance for rice production.Bmc Plant Biol. 2020; https://doi.org/10.1186/s12870-020-02689-6Google Scholar). The potential of introgression of new wild rice maternal genomes into rice has not been explored, but may provide an opportunity to achieve adaptation to the specific environments in which the wild rices have evolved. Rice has been an important model plant genome for the grasses because of the relatively small diploid genome. While the rice genome extended our knowledge of genomes from the model plant, Arabidopsis, to a model that was also a major food crop, wild species from the Oryza genus extend the utility of the model into a large gene pool. The wild rices include species with many useful traits that allow the study of plant response to biotic and abiotic stresses. Despite these advantages wild rice species have been poorly studied, in some cases due to difficulty in accessing poorly collected and characterized populations. Wild rice research can make a major contribution to understand the history of human societies in domesticating plants to produce crops. The processes that were involved in the domestication of rice have been investigated by analysis of domesticated genotypes, but the study of the phenotypic traits of wild rices may be more informative (Ishikawa et al., 2020Ishikawa R. Castillo C.C. Fuller D.Q. Genetic evaluation of domestication-related traits in rice: implications for the archaeobotany of rice origin.Archaeological Anthropological Sci. 2020; 12: 197https://doi.org/10.1007/s12520-020-01112-3Google Scholar). The evolution of the Oryza genus has involved dispersal around the tropical world, divergence by geographic isolation, and introgression events resulting from long-distance dispersal. The presence of apparent inter-specific hybrids in the wild confirms the ongoing flow of genes between wild populations (Moner et al., 2018Moner A.M. Furtado A. Chivers I. Fox G. Crayn D. Henry R.J. Diversity and evolution of rice progenitors in Australia.Ecol. Evol. 2018; 8: 4360-4366https://doi.org/10.1002/ece3.3989Google Scholar). The original rice genome has been continuously improved, as has the genomes of the wild Oryza. In 20 years, sequencing technology has improved greatly with major advances allowing more continuous and accurate sequences (Stein et al., 2018Stein J.C. Yu Y. Copetti D. Zwickl D.J. Zhang L. Zhang C. Chougule K. Gao D. Iwata A. Goicoechea J.L. et al.Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza.Nat. Genet. 2018; 50: 285https://doi.org/10.1038/s41588-018-0040-0Google Scholar). Large-scale sequencing of the diversity of domesticated genotypes has been undertaken (Rellosa et al., 2014Rellosa M.C. Reano R.A. Capilit G.L.S. de Guzman F.C. Ali J. Hamilton N.R.S. Mauleon R.P. Alexandrov N.N. Leung H. Project R.G. The 3,000 rice genomes project.Gigascience. 2014; https://doi.org/10.1186/2047-217x-3-7Google Scholar). Genomes of some wild Oryza have been characterized but more needs to done. Current technology should allow very efficient de novo sequencing of wild Oryza and re-sequencing of diversity in wild populations. A pan genome (Tao et al., 2018Tao Y. Zhao X. Mace E. Henry R. Jordan D. Exploring and exploiting pan-genomics for crop improvement.Mol. Plant. 2018; https://doi.org/10.1016/j.molp.2018.12.016Google Scholar) for not only domesticated rice but a super pan genome for the whole genus is highly desirable as a platform for rice food security. High-throughput re-sequencing has become more cost effective. However, de novo genome sequencing is required to capture the structural differences within species and to define differences in gene content in the population. Recently de novo chromosome level assembly has become increasingly more achievable as long-read sequencing technologies have advanced (Murigneux et al., 2020Murigneux V. Rai S.K. Furtado A. Bruxner T.J.C. Tian W. Harliwong I. Wei H. Yang B. Ye Q. Anderson E. et al.Comparison of long-read methods for sequencing and assembly of a plant genome.Gigascience. 2020; 9https://doi.org/10.1093/gigascience/giaa146Google Scholar; Sharma et al., 2021Sharma P. Alsubaie B. Al-Mssallem I. Nath O. Mitter N. Rodrigues Alves Margarido G. Topp B. Murigneux V. Kharabian Masouleh A. Furtado A. et al.Improvements in the sequencing and assembly of plant genomes.Gigabyte. 2021; https://doi.org/10.46471/gigabyte.24Google Scholar). These developments suggest that de novo genome sequencing and assembly will become a relatively simple inexpensive and routine process making much more widespread analysis of wild rice genomes feasible. Advances in high-throughput phenotyping also have the potential to contribute greatly to increased knowledge and use of wild rice especially imaging that may be applied to collect phenotypic data directly on a large scale in wild populations. The introgression of novel genes and alleles from wild rices provides a key opportunity to re-invent rice to adapt production to climate change and the food demands of future human populations. This approach has not been attractive in traditional plant breeding due to the transfer of undesirable traits with the gene of interest. Many novel strategies are available. An early attempt demonstrated the potential to use direct DNA transfer to more genes from Zizania into rice (Abedinia et al., 2000Abedinia M. Henry R. Blakeney A. Lewin L.G. Accessing genes in the tertiary gene pool of rice by direct introduction of total DNA from Zizania palustris (wild rice).Plant Mol. Biol. Reporter. 2000; 18: 133-138https://doi.org/10.1007/BF02824021Google Scholar). This approach remains an option if the genes for the trait are unknown. Advances in genomic resulting in the characterization of genes make more targeted gene transfer possible by transgenic approaches. Gene editing in rice (Bi and Yang, 2017Bi H.H. Yang B. Gene editing with TALEN and CRISPR/Cas in rice.Prog. Mol. Biol. Transl. 2017; 149: 81-98https://doi.org/10.1016/bs.pmbts.2017.04.006Google Scholar; He et al., 2019He Y.B. Zhu M. Wang L.H. Wu J.H. Wang Q.Y. Wang R.C. Zhao Y.D. Improvements of TKC technology accelerate isolation of transgene-free CRISPR/Cas9-edited rice plants.Rice Sci. 2019; 26: 109-117https://doi.org/10.1016/j.rsci.2018.11.001Google Scholar) may be the most direct way to introduce a gene from a wild rice when the gene is known. Genes for useful traits in wild populations include those for resistance to pests and diseases, photosynthetic efficiency, salt tolerance, and starch chemistry, which may determine digestibility and nutrient use efficiency. A more radical option is to domesticate wild rices as new crop options. Growing knowledge of the genes that have been selected in rice domestication make this an increasingly feasible option. This provides a pathway to rapid development of a crop well adapted to the region in which the wild rice evolved, potentially extending the range of environments over which rice can be produced. Hotter, colder, dryer, or more saline environments may need to be utilized and adaption to greater environmental variation may be essential. For example, O. coarctata is highly salt-tolerant species and as such represents a potential source of salt-tolerance genes that could be transferred into domesticated rice. The alternative approach would be to domesticate O. coarctata directly to produce a salt-tolerant rice crop by incorporating genes from domesticated rice. The relative value of these two approaches will depend upon the number and complexity of the gene transfers required. A pathway to domestication of an allotetraploid rice species, O. alta, was recently advanced using knowledge of the genome and gene editing (Yu et al., 2021Yu H. Lin T. Meng X. Du H. Zhang J. Liu G. Chen M. Jing Y. Kou L. Li X. et al.A route to de novo domestication of wild allotetraploid rice.Cell. 2021; 184: 1156-1170https://doi.org/10.1016/j.cell.2021.01.013Google Scholar). This provides a completely new option for rice production based upon a more biomass production and greater tolerance of abiotic and biotic stresses. Genome analysis has revealed many of the key genes involved in the domestication process (Stein et al., 2018Stein J.C. Yu Y. Copetti D. Zwickl D.J. Zhang L. Zhang C. Chougule K. Gao D. Iwata A. Goicoechea J.L. et al.Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza.Nat. Genet. 2018; 50: 285https://doi.org/10.1038/s41588-018-0040-0Google Scholar; Yu et al., 2021Yu H. Lin T. Meng X. Du H. Zhang J. Liu G. Chen M. Jing Y. Kou L. Li X. et al.A route to de novo domestication of wild allotetraploid rice.Cell. 2021; 184: 1156-1170https://doi.org/10.1016/j.cell.2021.01.013Google Scholar). The genetic control of these traits has proven to be complex but is being defined (Ishikawa et al., 2020Ishikawa R. Castillo C.C. Fuller D.Q. Genetic evaluation of domestication-related traits in rice: implications for the archaeobotany of rice origin.Archaeological Anthropological Sci. 2020; 12: 197https://doi.org/10.1007/s12520-020-01112-3Google Scholar). These advances pave the way for domestication of new rice types and other diverse plant species to provide new crop options in support of food security. Greatly increased efforts to conserve wild rice germplasm are required both ex situ and in situ. Wild rice populations are under threat from many factors. In Asia much of the habitat of rice has been displaced by agriculture or other human activities. Gene flow between domesticated rices and wild populations is an ongoing threat to the genetic diversity in the wild (Choi et al., 2017Choi J.Y. Platts A.E. Fuller D.Q. Hsing Y.L. Wing R.A. Purugganan M.D. The rice paradox: multiple origins but single domestication in Asian rice.Mol. Biol. Evol. 2017; 34: 969-979https://doi.org/10.1093/molbev/msx049Google Scholar). Competition with invasive weeds is also a challenge in more remote populations as human development and movement increases (Henry et al., 2010Henry R. Rice N. Waters D. Kasem S. Ishikawa R. Hao Y. Dillon S. Crayn D. Wing R. Vaughan D. Australian oryza: utility and conservation.Rice. 2010; 3: 235-241https://doi.org/10.1007/s12284-009-9034-yGoogle Scholar). Many wild rice populations are not represented in any ex situ collections. Climate change threatens the continued survival of many current populations. Wild rices and their genetics are likely to be a significant contributor to future sustainable rice production. Rice needs to be produced with less water, be more resistant to new pests and diseases, have greater resistance to abiotic stresses and deliver improved health and nutrition to consumers. Rice may also need to be adapted to production in new regions due to climate change. Wild rices are a source of all of these traits. No conflict of interest declared.