Pathways to de novo domestication of crop wild relatives

Authors: Curtin, Shaun; QI, YIPING - University Of Maryland; PERES, LAZARO E.P. - Universidad De Sao Paulo; FERNIE, ALISDAIR - Max Planck Institute Of Molecular Plant Physiology; ZSOGON, AGUSTIN - Universidade Federal De Vicosa

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/3/2021
Publication Date: 11/27/2021
Citation: Curtin, S.J., Qi, Y., Peres, L., Fernie, A.R., Zsogon, A. 2021. Pathways to de novo domestication of crop wild relatives. Plant Physiology. 188(4):1746-1756. https://doi.org/10.1093/plphys/kiab554.
DOI: https://doi.org/10.1093/plphys/kiab554

Interpretive Summary: The domestication of wild species has led to a wide variety of crops adapted to a range of climates allowing the expansion of cultivation to larger areas and over longer periods leading to higher yields. Up until recently, both domestication and breeding occurred empirically with little understanding of the underlying biological mechanisms. However we know that genetic variation is created by mutation and that breeding operates by stacking favourable mutations in a single plant through recombination. Future technical advances will allow controlled manipulation of mutation and recombination and the creation of novel crops by targeted modification of the genomes of wild species. These new tools will aid the acceleration of the improvement of traditional, semi-domesticated ‘orphan’ crops that perform poorly in modern agricultural systems and help broaden the narrow genetic basis on which humankind currently relies. Combining classical archeaobotany and genetics with high-throughput genomics and the increasingly powerful gene editing toolkits will facilitate the domestication of crop wild relatives and other lesser-known plant species that are more resilient, nutritious, and productive in a given environment. This review discusses recent progress in the understanding of crop domestication and technical breakthroughs in gene editing technology and how they can be combined to produce better crops for the future.

Technical Abstract: The domestication of wild species led to a wide variety of crops adapted to a range of climatic and edaphic conditions, which allowed expansion of cultivation to larger areas and over longer periods. Subsequent crop breeding led to higher yields and facilitated population growth. Until recent times, both domestication and breeding occurred empirically with little understanding of the underlying biological mechanisms. Today, we know that genetic variation is created by mutation and that breeding operates by stacking favourable mutations in a single plant through recombination. Technical advances will eventually allow controlled manipulation of mutation and recombination, and thus creation of novel crops by targeted modification of the genomes of wild species. Such tools will also aid in accelerating the improvement of traditional, semi-domesticated ‘orphan’ crops that perform poorly in modern agricultural systems and thus help broaden the narrow genetic basis on which humankind currently relies. Furthermore, recent breakthroughs have shown that targeted control of gene expression is an even faster avenue to produce desirable phenotypes, thus bypassing the need for mutation and recombination. However, the deliberate effort to create new crops or improve existing ones requires a thorough understanding of the genetic basis of domestication. The synergistic combination of classical archeaobotany and genetics with high-throughput genomics is revealing that a variety of different processes may have operated in the domestication of crops. This knowledge, combined with increasingly powerful gene editing toolkits, sets the stage for the continual domestication of crop wild relatives and other lesser-known plant species by defining an ideal plant type (‘ideotype’) that is more resilient, nutritious, and productive in a given environment. Proof-of-concept for the potential of this de novo domestication approach was provided by the use of gene editing to create agronomically important traits in wild relatives of the tomato, the orphan crop Physalis and, more recently, in an artificially polyploidized wild rice. Here, we review how recent progress in the understanding of crop domestication and technical breakthroughs in gene editing technology could be combined to produce better crops for the future.