COMMENTARY Rewiring the wheat reproductive system to harness heterosis for the next wave of yield improvement Piotr Gornickia,1 and Justin D. Farisb aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637; and bCereal Crops Research Unit, Northern Crop Science Laboratory, Agricultural Research Service, US Department of Agriculture, Fargo, ND 58102

Bread wheat (hexaploid Triticum aestivum) emmer that hybridized with goatgrass about provides an extraordinary 10,000-y story of 8,000 y ago (3), probably southeast of the a new species, established by early farmers, Caspian Sea, that resulted in the first hexa- selecting for simple agronomical traits to fa- ploid bread wheat (4). cilitate efficient and plentiful grain harvest. During most of the last 10,000 y, farmers The genetic changes underlying wheat domes- grew wheat in heterogenic stands consisting of tication over thousands of years, however, mixed genotypes and ploidy levels. The first included not just a collection of beneficial bread wheat captured genetic variation from single gene mutations, but also introgres- the two progenitors, but subsequent hybrid sions and whole genome duplication. The swarms allowing for gene flow and increased hexaploidization event occurred spontane- genetic variation occurred in such stands. ously in nature, but the resulting wild spe- During this time, the geographical range of cies did not survive; it is known only in wheat expanded dramatically as it acquired its domesticated form. Evolutionary bottle- adaptation to extreme environments and ad- neck(s) reduced genetic variation of the spe- ditional competitive traits such as increased cies, and it was introduced broadly outside tillering, increased height, and wide leaves (5). its native geographical range and habitat. Only in the last 100 y has wheat been Nevertheless, modern breeding programs grown in vast monocultures where modern delivered high-yield elite cultivars, which are plant breeding practices have led to the planted in most major wheat-producing areas development of high performance varieties of the world. In the face of quickly declining grown over large acreages. As a result of plant arable land expansion and challenges from breeding, these modern varieties contain climate change, the following question superior allelic combinations that have led arises: where can we find the next wave to traits such as increased yield, erect leaves, Fig. 1. Heterosis (hybrid plant vigor) has not yet of increase in yield and global production increased disease and pest resistance, lodging been systematically explored and extensively utilized of wheat? In PNAS, Kempe et al. (1) de- resistance, reduced height, improved harvest for wheat yield improvement. Only 1% of wheat seeds planted worldwide are hybrid. Bread wheat is an autoga- scribe molecular engineering of an elegant index, and enhanced response to fertilizers mous (self-pollinating) species creating a natural barrier to male sterility–fertility restoration system for (5). However, reduced genetic diversity has hybrid seed production. Self-pollination occurs quickly pri- the exploration of heterosis (hybrid plant diminished the potential of wheat to evolve marily within the same floret (spikelet), pollen is short-lived vigor) in wheat. In the future, this system further and adapt to changing environ- and is shed before or when the flower starts to open, could facilitate introduction of hybrid seeds ments. Although the frequency of most flowers have closed architecture. As a result, cross-pollination is more than an order of magnitude less frequent than self- on a large scale. adapted alleles has increased, other poten- pollination. Engineering cross-pollination (allogamy) for Emmer wheat, one of the eight founder tially adaptive alleles have been lost (6). hybrid seed production requires modification of the re- crops domesticated in the Middle East about Tomeetthedemandofninebillionpeople productive system: engineering male-sterility of the female 10,000 y ago, was instrumental in spawning expected by 2050, estimated annual wheat crossing partner (self-incompatibility) to prevent self-pollina- the Agricultural Revolution. The transition of production needs to increase at a rate of tion and fertility restoration required for seed-producing crop wild to cultivated emmer initiated the exten- about 1.6%/y, but it has only increased at plants as well as increased shedding of viable pollen and open flower architecture to allow more efficient cross-polli- sive genetic restructuring of domesticated a rate of less than 1%/y in recent decades. nation. Heterotic pools of preferred crossing partners have to wheat, primarily involving mutations that These increases will need to be made without be established. Photograph by Jon Raupp, Kansas State resulted in the transition of types with natural an expansion of arable land, in a changing University. seed dispersal mechanisms (brittle spikes) to global climate that will yield increased tem- types with a nonbrittle rachis (2). The initial peratures, CO2, and ozone levels, increased transition from the wild habitat to cultivated frequency of droughts and other extreme Author contributions: P.G. and J.D.F. wrote the paper. fields also involved selection for free-thresh- weather events, and alterations in virulence The authors declare no conflict of interest. ing seeds, nondormant seeds, uniform and of pathogens and pests, and also enhanced See companion article on page 9097. rapid germination, erect plants, and increased pressure to use less synthetic fertilizers, 1To whom correspondence should be addressed. E-mail: pg13@ grain size. It was a domesticated derivative of pesticides, and fossil fuels. Fortunately, uchicago.edu.

9024–9025 | PNAS | June 24, 2014 | vol. 111 | no. 25 www.pnas.org/cgi/doi/10.1073/pnas.1407956111 Downloaded by guest on October 1, 2021 numerous avenues exist for the improvement incompatibility. The split-gene feature is re- What is next? The system needs to be tested COMMENTARY of wheat productivity. Agronomic practices quired for fertility restoration to allow on a larger scale and include field trials. It can can be improved by developing more effi- propagation of the engineered parental lines then provide an important tool for establishing cient and environment-friendly fertilizers and in plants grown from hybrid seeds, heterotic pools of genetically divergent germ- and methods of weed and pest control. The which is essential for grain crops like wheat. plasm to streamline selection of crossing part- genetic diversity of wild wheat relatives can The two parts of the split gene encode the ners to maximize the grain yield of hybrid lines, be harnessed to identify and deploy new N-terminal and the C-terminal part of barnase, at the same time preventing loss of agricultur- adaptive alleles and genes for pest resistance, respectively, each fused to the intein domain for ally important traits of the elite lines. Better agronomic performance, and enhanced end- spontaneous ligation of the two independently understanding of the molecular mechanisms use quality. Plant physiology may be manip- expressed protein fragments to form the func- underlying heterosis in wheat could be sought. ulated to potentially increase photosynthetic tional enzyme. Their coexpression occurs A well-established male sterility system could capacity and radiation use efficiency for in- in the heterozygous progeny of a cross also be instrumental in the exploration of creased wheat yields (7). The use of modern between two parent plants, each carrying a wheat genetic variation and in molecular and molecular tools such as high-throughput different part of the split gene. The male-sterile engineering to attain more open flower archi- phenotyping and genotyping can maximize femalecrossingpartneristhusestablished. tecture and more efficient shedding of progeny screening and selection leading Its pollination with an unmodified male cross- viable pollen, both features important for to more efficient production of superior ing partner to produce hybrid seeds restores further enhancement of cross-pollination varieties (8). Whole genome DNA sequen- fertility as well, as the two split gene compo- frequency. All wheat (Triticum) species ces will provide a solid framework for the nents segregate. Furthermore, insertion of the (diploid, tetraploid, and hexaploid) are development of new molecular strategies two split gene components at the same locus autogamous, as isAegilops tauschii (goatgrass), (9). Biotechnology and genetically modi- of homologous chromosomes (linkage in which donated its genome to hexaploid fied (GM) wheat, when globally accepted, repulsion) eliminates recombination as wheat. Aegilops speltoides,whichdonated would provide another means to potentially its genome to tetraploid wheat and is the a source of unwanted genotypes. It requires achieve advances. Finally, the capture of het- source of the cytoplasm for all polyploid an additional engineering step to separate erosis by the development of wheat hybrids wheats, however, is allogamous. A robust the two components of the split gene may provide yet another method to meet hybrid seed production system is likely to system, which initially are inserted into the growing demand. require both molecular engineering and the genome together, but then one or the The autogamous (self-pollinating) nature introduction of desirable traits from wheat of wheat makes hybrid wheat development other is deleted from the locus by the action and its relatives. significantly more challenging than naturally of a site-specific recombinase (integrase). Although the split-gene system described by outcrossing crops (Fig. 1). Hybrid wheat has The multicomponent modern molecular Kempe et al. is a significant advancement for been a subject of intense focus in the last engineering concept is very well thought out the science of hybrid wheat production, the decades, especially in the 1970s and again and its potential applications go beyond just technology involves genetic engineering to de- in the 1990s. Now, it is again receiving hybrid seed production. The system has signif- velopwhatisconsideredtobeGMwheat, much attention mainly due to the need to icant features, not otherwise available for wheat. which is yet unaccepted by a significant portion increase productivity in a changing climate. Only the female crossing partner has to be of the world market. Indeed the consequences The same obstacles that hindered hybrid modified. Once it is available, crosses with of producing hybrid wheat as described need wheat production in the past remain today. many male partners can be tested for vigor to be considered. Will it affect the end-use Farmers typically save a portion of their and overall performance. The engineered pa- products or pose a health risk to the consumer? farm-produced wheat seed for planting the rental lines can be maintained easily. There is Would escape of the “transgenes” into conven- following year, thus precluding the purchase no need for any additional steps to restore tional varieties, breeding lines, germplasm, or of seed every year. Hybrid seed, however, can- fertility. There is no need for chemical treat- wild relatives of wheat lead to unwanted sterility not be saved and must be repurchased each ments. Establishing a single male-sterile female or expression of barnase or other problems? year. The economic returns for raising wheat crossing line required a substantial amount of These concerns need to be given careful con- hybrids must outweigh the cost of purchasing work, because of the complex multistep design, sideration before the technology is used to pro- seed each year despite the relatively low levels but the strategy worked as expected. Good duce hybrid wheat seed on a commercial scale. of heterosis compared with crops such as corn. strategies have been proposed to overcome the However, as long as the concerns are consid- From a technical standpoint, one primary ob- inefficiency. Large-scale hybrid breeding pro- ered on scientific bases, the work by Kempe stacle has been the development of an efficient gramandcommercialhybridseedproduction et al. will move the field forward and provide and effective male-sterile system. The wheat will certainly require additional improvements, a step toward achieving the ability to feed the hybrids produced to date almost all rely but this study provides a significant launch. world’s ever expanding population. on the use of chemical hybridization agents (CHAs) or cytoplasmic male sterility (CMS), but both systems have significant difficulties (1). 1 Kempe K, Rubtsova M, Gils M (2014) Split-gene system for 5 Feldman M (2001) Origin of cultivated wheat. The World Wheat The report by Kempe et al. describes hybrid wheat seed production. Proc Natl Acad Sci USA Book. A History of Wheat Breeding, eds Bonjean AP, Angus WJ 111:9097–9102. (Lavoisier Publishing, Paris), pp 3–56. a successful proof-of-concept experiment 2 Faris JD (2014) Wheat Domestication: Key to Agricultural 6 Charmet G (2011) Wheat domestication: Lessons for the future. C aimed at developing a universal male sterility Revolutions Past and Future. Genomics of Plant Genetic Resources, R Biol 334(3):212–220. system for hybrid seed production and thus eds Tuberosa R, Graner A, Frison E (Springer, Houten, The 7 Reynolds M, et al. (2012) Achieving yield gains in wheat. Plant Cell takes a big step toward addressing a major Netherlands), pp 439–464. Environ 35(10):1799–1823. 3 Huang S, et al. (2002) Genes encoding plastid acetyl-CoA 8 Paux E, Sourdille P, Mackay I, Feuillet C (2012) Sequence-based technical issue associated with the develop- carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops marker development in wheat: Advances and applications to ment of hybrid seed production for wheat. It complex and the evolutionary history of polyploid wheat. Proc Natl breeding. Biotechnol Adv 30(5):1071–1088. uses a split-gene strategy for tapetum-specific Acad Sci USA 99(12):8133–8138. 9 Choulet F, et al. (2014) The wheat black jack: Advances towards 4 McFadden ES, Sears ER (1946) The origin of Triticum sequencing the 21 chromosomes of bread wheat. Genomics of Plant expression of phytotoxic barnase (an RNase) spelta and its free-threshing hexaploid relatives. J Hered Genetic Resources, eds Tuberosa R, Graner A, Frison E (Springer, Houten, to force pollen ablation and plant self- 37:81–89, 107. The Netherlands), pp 405–438.

Gornicki and Faris PNAS | June 24, 2014 | vol. 111 | no. 25 | 9025 Downloaded by guest on October 1, 2021