Rewiring the wheat reproductive system to harness heterosis for the next wave of yield improvement.

Bread wheat (hexaploid Triticum aestivum) provides an extraordinary 10,000-y story of a new species, established by early farmers, selecting for simple agronomical traits to facilitate efficient and plentiful grain harvest. The genetic changes underlying wheat domestication over thousands of years, however, included not just a collection of beneficial single gene mutations, but also introgressions and whole genome duplication. The hexaploidization event occurred spontaneously in nature, but the resulting wild species did not survive; it is known only in its domesticated form. Evolutionary bottleneck(s) reduced genetic variation of the species, and it was introduced broadly outside its native geographical range and habitat. Nevertheless, modern breeding programs delivered high-yield elite cultivars, which are planted in most major wheat-producing areas of the world. In the face of quickly declining arable land expansion and challenges from climate change, the following question arises: where can we find the next wave of increase in yield and global production of wheat? In PNAS, Kempe et al. (1) describe molecular engineering of an elegant male sterility–fertility restoration system for the exploration of heterosis (hybrid plant vigor) in wheat. In the future, this system could facilitate introduction of hybrid seeds on a large scale. Emmer wheat, one of the eight founder crops domesticated in the Middle East about 10,000 y ago, was instrumental in spawning the Agricultural Revolution. The transition of wild to cultivated emmer initiated the extensive genetic restructuring of domesticated wheat, primarily involving mutations that resulted in the transition of types with natural seed dispersal mechanisms (brittle spikes) to types with a nonbrittle rachis (2). The initial transition from the wild habitat to cultivated fields also involved selection for free-threshing seeds, nondormant seeds, uniform and rapid germination, erect plants, and increased grain size. It was a domesticated derivative of emmer that hybridized with goatgrass about 8,000 y ago (3), probably southeast of the Caspian Sea, that resulted in the first hexaploid bread wheat (4). During most of the last 10,000 y, farmers grewwheat in heterogenic stands consisting of mixed genotypes and ploidy levels. The first bread wheat captured genetic variation from the two progenitors, but subsequent hybrid swarms allowing for gene flow and increased genetic variation occurred in such stands. During this time, the geographical range of wheat expanded dramatically as it acquired adaptation to extreme environments and additional competitive traits such as increased tillering, increased height, and wide leaves (5). Only in the last 100 y has wheat been grown in vast monocultures where modern plant breeding practices have led to the development of high performance varieties grown over large acreages. As a result of plant breeding, these modern varieties contain superior allelic combinations that have led to traits such as increased yield, erect leaves, increased disease and pest resistance, lodging resistance, reduced height, improved harvest index, and enhanced response to fertilizers (5). However, reduced genetic diversity has diminished the potential of wheat to evolve further and adapt to changing environments. Although the frequency of most adapted alleles has increased, other potentially adaptive alleles have been lost (6). To meet the demand of nine billion people expected by 2050, estimated annual wheat production needs to increase at a rate of about 1.6%/y, but it has only increased at a rate of less than 1%/y in recent decades. These increases will need to be made without an expansion of arable land, in a changing global climate that will yield increased temperatures, CO2, and ozone levels, increased frequency of droughts and other extreme weather events, and alterations in virulence of pathogens and pests, and also enhanced pressure to use less synthetic fertilizers, pesticides, and fossil fuels. Fortunately, Fig. 1. Heterosis (hybrid plant vigor) has not yet been systematically explored and extensively utilized for wheat yield improvement. Only 1% of wheat seeds planted worldwide are hybrid. Bread wheat is an autogamous (self-pollinating) species creating a natural barrier to hybrid seed production. Self-pollination occurs quickly primarily within the same floret (spikelet), pollen is short-lived and is shed before or when the flower starts to open, flowers have closed architecture. As a result, cross-pollination is more than an order of magnitude less frequent than selfpollination. Engineering cross-pollination (allogamy) for hybrid seed production requires modification of the reproductive system: engineering male-sterility of the female crossing partner (self-incompatibility) to prevent self-pollination and fertility restoration required for seed-producing crop plants as well as increased shedding of viable pollen and open flower architecture to allow more efficient cross-pollination. Heterotic pools of preferred crossing partners have to be established. Photograph by Jon Raupp, Kansas State University.