Pathways to de novo domestication of crop wild relatives

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 (Evans, 1998). 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 favorable mutations in a single plant through recombination. Technical advances will eventually allow controlled manipulation of mutation and recombination (Taagen et al., 2020; Nasti and Voytas, 2021), and thus de novo domestication of wild species by targeted modification of their genomes (Gasparini et al., 2021). Such tools will also aid in accelerating the improvement of traditional, semi-domesticated “orphan” crops that perform poorly in modern agricultural systems (Tadele, 2019). The combination of these approaches will help broaden the narrow genetic basis of crops on which humankind currently relies (Milla and Osborne, 2021). Furthermore, recent breakthroughs have shown that targeted control of gene expression is an even faster avenue to produce desirable phenotypes (Pan et al., 2021a), 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 (Kantar et al., 2017). The synergistic combination of classical archeaobotany and genetics (Denham et al., 2020) with high-throughput genomics (Purugganan and Jackson, 2021) 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 (Zsögön et al., 2017). Wild plants that are naturally resistant to biotic (insects and diseases) and tolerant of abiotic (drought and heat) stresses can be selected and manipulated by introducing mutations that mimic the domestication events that led to improved yield and agronomic performance of the major crops of today. Proof-of-concept for the potential of this de novo domestication approach was provided using gene editing to create agronomically important traits in wild relatives of the tomato (Solanum lycopersicum) (Li et al., 2018; Zsögön et al., 2018), the orphan crop Physalis (Lemmon et al., 2018) and, more recently, in a polyploid wild relative of rice (Oryza species) (Yu et al., 2021). 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.