The magic of genomics in creating hybrid potato

Abstract

Heterosis is a phenomenon where hybrids have superior performance over their parents. As an efficient way to increase crop yield, heterosis is of great importance on agriculture production. Therefore, hybrid breeding has been widely used in maize and rice for several decades, where the elite hybrid is developed by crossing two inbred lines (Liu et al., 2020Liu J. Li M. Zhang Q. Wei X. Huang X. Exploring the molecular basis of heterosis for plant breeding.J. Integr. Plant Biol. 2020; 62: 287-298Crossref PubMed Scopus (52) Google Scholar). However, in many outcrossing plants, it is not easy to create genetic diverse inbred lines of both high genomic homozygosity and vigor due to self-incompatibility and inbreeding depression (Chen et al., 2021Chen M. Fan W. Ji F. Hua H. Liu J. Yan M. Ma Q. Fan J. Wang Q. Zhang S. et al.Genome-wide identification of agronomically important genes in outcrossing crops using OutcrossSeq.Mol. Plant. 2021; 14: 556-570Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar). S-RNase-based self-incompatibility has been found in previous genetic studies, and is probably the most widespread mechanism in plants (Takayama and Isogai, 2005Takayama S. Isogai A. Self-incompatibility in plants.Annu. Rev. Plant Biol. 2005; 56: 467-489Crossref PubMed Scopus (454) Google Scholar). With the knowledge of S-RNase, transitions from self-incompatibility to self-compatibility are now feasible in several plants by knocking out S-RNase genes (Ye et al., 2018Ye M. Peng Z. Tang D. Yang Z. Li D. Xu Y. Zhang C. Huang S. Generation of self-compatible diploid potato by knockout of S-RNase.Nat. Plants. 2018; 4: 651-654Crossref PubMed Scopus (85) Google Scholar) or searching for S-RNase natural mutants (Zhang et al., 2019Zhang C. Wang P. Tang D. Yang Z. Lu F. Qi J. Tawari N.R. Shang Y. Li C. Huang S. The genetic basis of inbreeding depression in potato.Nat. Genet. 2019; 51: 374-378Crossref PubMed Scopus (58) Google Scholar). Moreover, through extensive genetic and genomic studies, it is now considered that inbreeding depression is largely caused by multiple deleterious recessive alleles (Charlesworth and Willis, 2009Charlesworth D. Willis J.H. The genetics of inbreeding depression.Nat. Rev. Genet. 2009; 10: 783-796Crossref PubMed Scopus (1107) Google Scholar). Genetic mapping coupled with genome sequencing can be used to identify the major-effect deleterious mutations, which can be eliminated by molecular breeding. Although avoiding self-incompatibility and inbreeding depression has been considered theoretically feasible, the development of inbred lines and elite hybrids in many outcrossing crops are technically difficult in practice. Excitingly, Zhang et al., 2021Zhang C. Yang Z. Tang D. et al.Genome design of hybrid potato.Cell. 2021; https://doi.org/10.1016/j.cell.2021.06.006Abstract Full Text Full Text PDF Scopus (23) Google Scholar took potato as a proof of concept, and successfully created seed-propagated diploid hybrid potatoes by genetic and genomic approaches. Potato (Solanum tuberosum) is a very important crop that feeds 1.3 billion people worldwide. The vast majority of cultivated potatoes are outbred autotetraploids and strongly rely on clonal propagation (Figure 1, blue panel). The maintenance of potato vegetative stocks is often constrained by diseases. Moreover, given the complicated inheritance patterns of autotetraploids and unpredictable phenotypic performance of offspring derived from outbred parents, the breeding efficiency of potatoes has also been proven to be limited at the tetraploid level for clone propagation (Stokstad, 2019Stokstad E. The new potato.Science. 2019; 363: 574-577Crossref PubMed Scopus (50) Google Scholar). Hence, the development of diploid inbred lines for hybrid breeding and seed propagation has been a longstanding goal for the potato-growing community. To achieve the dream, Zhang et al., 2021Zhang C. Yang Z. Tang D. et al.Genome design of hybrid potato.Cell. 2021; https://doi.org/10.1016/j.cell.2021.06.006Abstract Full Text Full Text PDF Scopus (23) Google Scholar harnessed the power of genomics and disassembled the goal into four steps. The four steps are: (1) selection of diploid lines with low genome heterozygosity and breaking of self-incompatibility, (2) identification of major-effect deleterious mutations, (3) development of inbred lines, and (4) generation of hybrid crosses (Figure 1, yellow panel). In the first step, Zhang et al., 2021Zhang C. Yang Z. Tang D. et al.Genome design of hybrid potato.Cell. 2021; https://doi.org/10.1016/j.cell.2021.06.006Abstract Full Text Full Text PDF Scopus (23) Google Scholar found that the starting material, with lower heterozygosity and less deleterious mutations, offers a greater potential for development into inbred lines. In the second step, the S1 populations were used to identify large-effect deleterious mutations through genome-wide segregation distortion analysis and bulked segregant analysis (Takagi et al., 2013Takagi H. Abe A. Yoshida K. Kosugi S. Natsume S. Mitsuoka C. Uemura A. Utsushi H. Tamiru M. Takuno S. et al.QTL-seq: rapid mapping of quantitative trait loci in rice by whole 890 genome resequencing of DNA from two bulked populations.Plant J. 2013; 74: 174-183Crossref PubMed Scopus (670) Google Scholar). In the third step, several highly homozygous inbred lines stacking beneficial alleles were selected by genome-assisted selection for each generation (from S1 to S5 populations). In the final step, the inbred lines derived from two clones are intercrossed to generate F1 hybrids. As expected, the hybrids (called "Upotato 1″ by Zhang et al.) showed strong heterosis in growth vigor and yield (31% yield increase over their parental lines). Taken together, Zhang et al., 2021Zhang C. Yang Z. Tang D. et al.Genome design of hybrid potato.Cell. 2021; https://doi.org/10.1016/j.cell.2021.06.006Abstract Full Text Full Text PDF Scopus (23) Google Scholar provided a tour de force study that successfully developed inbred lines to generate a hybrid potato, which is a milestone in potato breeding and has opened a new door for future breeding of hybrid potatoes—their approaches for generating diploid inbreeds will accelerate precise breeding designs and facilitate the use of benefits from strong heterosis and sexual reproduction in potatoes. As proven in this work, the genomics approach is now playing an increasingly important role in breeding. During recent decades, hundreds of quantitative trait loci and genes have been mapped or even functionally identified in many crops. Allelic variation on the agronomically important genes serves as the basis of genetic improvements (Wei et al., 2021Wei X. Qiu J. Yong K. Fan J. Zhang Q. Hua H. Liu J. Wang Q. Olsen K.M. Huang X. A quantitative genomics map of rice provides genetic insights and guides breeding.Nat. Genet. 2021; 53: 243-253Crossref PubMed Scopus (49) Google Scholar). Gene-level knowledge can be well applied in practical breeding by foreground selection (for target genes or loci). Also, background selections by screening for whole-genome heterozygosity can greatly help to increase the breeding efficiency—that is, selecting samples with least heterozygosity and ideal genotype in each generation. The concept has been well proven in rice (Wei et al., 2021Wei X. Qiu J. Yong K. Fan J. Zhang Q. Hua H. Liu J. Wang Q. Olsen K.M. Huang X. A quantitative genomics map of rice provides genetic insights and guides breeding.Nat. Genet. 2021; 53: 243-253Crossref PubMed Scopus (49) Google Scholar) and potato (Zhang et al., 2021Zhang C. Yang Z. Tang D. et al.Genome design of hybrid potato.Cell. 2021; https://doi.org/10.1016/j.cell.2021.06.006Abstract Full Text Full Text PDF Scopus (23) Google Scholar). Therefore, the genomic approach, with both foreground and background selections, will enable rational designs of new varieties in a fast and precise way. To deepen our understanding of heterosis and to boost hybrid breeding in potato, heterotic loci could be mapped to identify heterosis-related genes in potato. According to the genome sequences from two inbred lines, a large number of genetic differences could be found, some of which may explain the heterotic advantage of the F1 hybrid. Similar to the approach in hybrid rice (Huang et al., 2016Huang X. Yang S. Gong J. Zhao Q. Feng Q. Zhan Q. Zhao Y. Li W. Cheng B. Xia J. et al.Genomic architecture of heterosis for yield traits in rice.Nature. 2016; 537: 629-633Crossref PubMed Scopus (212) Google Scholar), F2 lines can be generated through selfing the potato F1 hybrid. The F2 population (with >1000 lines at best) can be genotyped and phenotyped, which will enable genetic dissections of the key loci or genes contributing to heterosis in potato and fine-scale evaluations of their heterotic effects. A deeper understanding of the genetic and molecular mechanisms on potato heterosis will be beneficial to potato hybrid breeding programs. In future, through genetic crosses and sexual reproduction, diploid potato inbreeds can be improved by well-designed breeding routes for yield, quality, resistance, and adaptation traits (Figure 1, green panel), similar to the routes used in rice, maize, and wheat. These efforts in the lab may eventually result in revolution in potato agricultural production in the near future.