Roadmap for Accelerated Domestication of an Emerging Perennial Grain Crop

Abstract

Current grain crops are annuals that must be sown every year, giving their root systems little time to develop during the growing season.A perennial grain crop with a long-lived extensive root system would improve soil quality, store carbon belowground, and utilize water and minerals more efficiently.Domestication genes of the annual grass wheat are highly conserved in the perennial intermediate wheatgrass (Thinopyrum intermedium), providing an opportunity for accelerated domestication of a perennial grain using a mutagenesis approach. Shifting the life cycle of grain crops from annual to perennial would usher in a new era of agriculture that is more environmentally friendly, resilient to climate change, and capable of soil carbon sequestration. Despite decades of work, transforming the annual grain crop wheat (Triticum aestivum) into a perennial has yet to be realized. Direct domestication of wild perennial grass relatives of wheat, such as Thinopyrum intermedium, is an alternative approach. Here we highlight protein coding sequences in the recently released T. intermedium genome sequence that may be orthologous to domestication genes identified in annual grain crops. Their presence suggests a roadmap for the accelerated domestication of this plant using new breeding technologies. Shifting the life cycle of grain crops from annual to perennial would usher in a new era of agriculture that is more environmentally friendly, resilient to climate change, and capable of soil carbon sequestration. Despite decades of work, transforming the annual grain crop wheat (Triticum aestivum) into a perennial has yet to be realized. Direct domestication of wild perennial grass relatives of wheat, such as Thinopyrum intermedium, is an alternative approach. Here we highlight protein coding sequences in the recently released T. intermedium genome sequence that may be orthologous to domestication genes identified in annual grain crops. Their presence suggests a roadmap for the accelerated domestication of this plant using new breeding technologies. Crop production is facing unprecedented challenges. In 2050, the human population will likely exceed nine billion [1.Food and Agriculture Organization of the United Nations The Future of Food and Agriculture: Trends and Challenges. FAO, 2017Google Scholar], increasing the demand for staple crops and livestock by 60% [2.Springmann M. et al.Options for keeping the food system within environmental limits.Nature. 2018; 562: 519-525Crossref PubMed Scopus (1143) Google Scholar]. Climate change is expected to drastically constrain plant productivity, necessitating the development of cultivars with increased tolerance to abiotic stresses such as heat, drought, soil salinization, and flooding. 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Annual crops must be sown every year, which disturbs the soil and exposes it to erosion through tillage or clearing of vegetation with herbicides. Furthermore, in the beginning of the growth season, the shallow root systems are inefficient at taking up water and nutrients, which is a major cause of ground and surface water pollution by nitrate leaching. A perennial grain crop that does not need to be sown every year would develop a long-lived deep root system (Figure 1A ) that sequesters carbon and takes up nutrients and water efficiently [7.Crews T.E. et al.Is the future of agriculture perennial? Imperatives and opportunities to reinvent agriculture by shifting from annual monocultures to perennial polycultures.Glob. Sustain. 2018; 1: 1-18Crossref Scopus (87) Google Scholar,8.Culman S.W. et al.Soil and water quality rapidly responds to the perennial grain Kernza wheatgrass.Agron. J. 2013; 105: 735-744Crossref Scopus (145) Google Scholar]. This crop could be intercropped with perennial legumes to provide additional ecosystem services such as nitrogen fixation [9.Ryan M.R. et al.Managing for multifunctionality in perennial grain crops.Bioscience. 2018; 68: 294-304Crossref PubMed Scopus (76) Google Scholar]. Furthermore, the large root systems, storage reserves, and stress tolerance of perennial ancestors in a perennial grain domestication (see Glossary) program would provide abundant mechanisms for developing new crops tolerant to a wide array of stresses [10.DeHaan L.R. et al.Perennial grain crops: a synthesis of ecology and plant breeding.Renew. Agric. Food Syst. 2005; 20: 5-14Crossref Scopus (111) Google Scholar]. Attempts to develop perennial wheat began in the 1930s, but have so far not produced a widely grown cultivar [11.DeHaan L.R. Ismail B.P. Perennial cereals provide ecosystem benefits.Cereal Foods World. 2017; 62: 278-281Crossref Scopus (39) Google Scholar]. In 1988, a Eurasian forage grass called intermediate wheatgrass (Thinopyrum intermedium), which is a close perennial relative of wheat, was selected as a promising perennial grain candidate at the Rodale Institute [12.Wagoner P. Perennial grain: new use for intermediate wheatgrass.J. Soil Water Conserv. 1990; 45: 81-82Google Scholar]. The intention was to create a productive grain crop through phenotypic selection within the species. Two cycles of breeding for improved grain production were completed in New York, USA, between 1990 and 2000 [13.DeHaan L. et al.Development and evolution of an intermediate wheatgrass domestication program.Sustainability. 2018; 10: 1-19Crossref PubMed Scopus (65) Google Scholar]. The Land Institute’s domestication program for intermediate wheatgrass began in 2003 and continues to the present time [13.DeHaan L. et al.Development and evolution of an intermediate wheatgrass domestication program.Sustainability. 2018; 10: 1-19Crossref PubMed Scopus (65) Google Scholar]. Eight generations of selecting and intermating the best plants based on their yield, seed size, shatter resistance, and other traits have been performed, resulting in improved populations of T. intermedium that are currently being evaluated and further selected at The Land Institute and by collaborators in diverse environments. However, these breeding approaches have not yielded T. intermedium varieties that would be profitable for farmers to produce at large scale. On-farm yields of T. intermedium varieties are currently less than 20% of that of wheat and seed mass is about 25% that of wheat seeds. The breeding program is currently focused on selecting for several traits, including yield, shatter resistance, free threshing ability, seed size, and grain quality. Although progress is steady, the urgent need to sustainably boost food production necessitates the development of methods to dramatically accelerate the pace of domestication. A high-quality genome sequence of T. intermedium (available at https://phytozome-next.jgi.doe.gov/info/Tintermedium_v2_1), which promises to facilitate future breeding approaches, was released in early 2019 by the US Department of Energy Joint Genome Institute. 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