Omics-based interdisciplinarity is accelerating plant breeding
Introduction
Food security has been one of the greatest priority considerations since the origin of humans. In turn, plant breeding, a major approach to increase the food supply, has become one of the oldest agricultural activities that parallels human civilization. Plant breeding has achieved three major technical innovations (artificial selection breeding, hybrid breeding, and molecular breeding) to date, with the fourth (optimal and precise design breeding) currently unfolding [1].
Approximately 10–12 thousand years ago, human ancestors learned to domesticate wild plants by selecting favorite lines based on their advantageous phenotypes such as loss of seed shattering from large numbers of progenitors [2]; thus, plant breeding started which constituted stage 1.0 (artificial selection breeding). This phenotype-based artificial selection breeding continued for thousands of years until the 19th century. In 1865, Mendel's laws were established [3]; thereafter, pedigree breeding based on hybridization was developed, with plant breeding entering stage 2.0 (hybrid breeding). In 1953, the structure of DNA was discovered, which caused life science to enter the molecular era [4], upon which new breeding approaches were developed, including marker-assisted selection (MAS) breeding [5] and genetically modified (GM) breeding [6]. These approaches switched plant breeding from sheer phenotype selection to a combination of genotype + phenotype selection, and plant breeding entered stage 3.0 (molecular breeding).
Innovations in plant breeding tremendously improved breeding efficiency and resulted in a greater food supply and in turn a growing population together the advances in farming mode and chemical fertilizers. For example, the wheat yield in the United Kingdom increased from 0.5 ton/hectare (ha) at the beginning of the 14th century to 1.8 ton/ha in the middle of the 19th century and then to 2.5 ton/ha in the middle of the 20th century (Figure 1, data from https://ourworldindata.org/). Consistent with this pattern, the world population grown from 0.4 to 1.3 billion, and then to 2.5 billion in these periods (Figure 1).
Nevertheless, the food supply remains far from our global needs [7]. Statistical data from the Food and Agriculture Organization of the United Nations (FAO) show that moderate or severe food insecurity has been growing slowly in the last six years. It was estimated that in 2020 nearly 2.37 billion people did not have access to adequate food, accounting for approximately 30% of the worldwide population. Among them, approximately 768 million people experienced hunger [8]. Furthermore, the global population is continuously increasing and is projected to reach 10 billion by 2050 [9] and over 11 billion by 2100 (Figure 1). In addition, water shortages, climate change and extreme weather events make crop production increasingly more difficult. Hence, to feed the increasing population, there is a call for new innovation in plant breeding (stage 4.0) that can quickly combine superior alleles with optimal and precise design [1]. Summarizing previous achievements reveals that each innovation is the result of introduction of new theories or technologies (Figure 1). The development of new technologies, particularly in omics-based interdisciplinarity, is making Breeding 4.0 on the cusp.
Section snippets
Genomic advances accelerate genetic dissection of complex traits
A prerequisite for precise design breeding is to link genotype with phenotype. Therefore, genetic dissection of agronomic traits and identification of the corresponding genotypic variations are essential. Owing to the multiple revolutions in DNA sequencing technologies in the last four decades, sequencing throughput and quality have improved significantly, and the cost is continuously decreasing, which greatly facilitates genome advances and functional studies [10].
Since the first plant genome
Phenomics makes precise phenotype characterization practicable
To link genotype with phenotype, precise characterizations of both are equally important. In contrast to the significant advances in genotyping, phenotyping has largely lagged behind because manual-based observation that was developed since plant breeding originated thousands of years ago remains predominant. Therefore, precise phenotyping has been a major technical bottleneck for next-generation breeding innovation [22,23].
Crop precise phenotyping is extremely complicated and difficult. First,
Panomics facilitates disclosure of how phenotypes are precisely determined
As mentioned above, plants exhibit phenotypic plasticity despite having the same genotype, which suggests that traits are not solely determined by genotype but are the result of interactions between genotype and the environment. To fulfill their functions, most genes need to be transcribed and translated, which are precisely regulated temporally and spatially. Therefore, whole-plant gene functions result in a dynamic landscape of different omics, including the epigenome, three-dimensional (3D)
Precise breeding calls for more interdisciplinary crosstalk
Precise plant breeding aims to quickly pyramid multiple desirable traits into a single variety as designed. Although advances in omics may help to reveal the precise genetic networks underlying different traits and to make precise breeding possible, it is far from sufficient. First, many complex traits are tightly integrated and exhibit heritable covariation [34, 35, 36]. Moreover, different alleles of the same gene show different functions, even in an opposite manner [37]. In addition, the
Conclusion
Challenges always accompany technological development. Developments in plant breeding technology have resulted in increased food production and growing population. In turn, the increasing population and declining resources necessitate a new breeding technology revolution to produce more food at a lower cost. Inspired by the re- or de novo domestication of new crops using genome editing [49, 50, ••51, ••52], we suspect that a clear dissection of complex traits with the help of omics-based
Funding
This work was supported by National Natural Science Foundation of China (31788103), the “Strategic Priority Research Program” of the Chinese Academy of Sciences (Grant No. XDA24030501), International Partnership Program of Chinese Academy of Sciences (IPP,153E11KYSB20190045), and the State Key Laboratory of Plant Cell and Chromosome Engineering (PCCE-KF-2019-05).
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this article.
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