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Apomixis in Plant Reproduction: a Novel Perspective on an Old Dilemma

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Apomixis in Plant Reproduction: a Novel Perspective on an Old Dilemma Plant Reprod (2013) 26:159–179 DOI 10.1007/s00497-013-0222-y REVIEW Apomixis in plant reproduction: a novel perspective on an old dilemma Gianni Barcaccia • Emidio Albertini Received: 9 May 2013 / Accepted: 23 June 2013 / Published online: 14 July 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com Abstract Seed is one of the key factors of crop produc- the mechanisms that regulate reproductive development in tivity. Therefore, a comprehension of the mechanisms plants. This knowledge is a necessary prerequisite to underlying seed formation in cultivated plants is crucial for understanding the genetic control of the apomictic process the quantitative and qualitative progress of agricultural and its deviations from the sexual process. Our molecular production. In angiosperms, two pathways of reproduction understanding of apomixis will be greatly advanced when through seed exist: sexual or amphimictic, and asexual or genes that are specifically or differentially expressed dur- apomictic; the former is largely exploited by seed com- ing embryo and embryo sac formation are discovered. In panies for breeding new varieties, whereas the latter is our review, we report the main findings on this subject by receiving continuously increasing attention from both sci- examining two approaches: i) analysis of the apomictic entific and industrial sectors in basic research projects. If process in natural apomictic species to search for genes apomixis is engineered into sexual crops in a controlled controlling apomixis and ii) analysis of gene mutations manner, its impact on agriculture will be broad and pro- resembling apomixis or its components in species that found. In fact, apomixis will allow clonal seed production normally reproduce sexually. In fact, our opinion is that a and thus enable efficient and consistent yields of high- novel perspective on this old dilemma pertaining to the quality seeds, fruits, and vegetables at lower costs. The molecular control of apomixis can emerge from a cross- development of apomixis technology is expected to have a check among candidate genes in natural apomicts and a revolutionary impact on agricultural and food production high-throughput analysis of sexual mutants. by reducing cost and breeding time, and avoiding the complications that are typical of sexual reproduction (e.g., Keywords Apomixis Plant reproduction Hybrids incompatibility barriers) and vegetative propagation (e.g., Seed production Á Á Á viral transfer). However, the development of apomixis technology in agriculture requires a deeper knowledge of Introduction Communicated by T. Dresselhaus. One of the greatest success stories in modern agriculture has A contribution to the Special Issue ‘‘HAPRECI—Plant Reproduction been the tremendous yield increase achieved by coupling Research in Europe.’’ high-yield varieties with high-input agronomic systems, creating the so-called Green Revolution. Approximately G. Barcaccia one-third of the world’s seed supply comes from the com- Laboratory of Genetics and Genomics, DAFNAE, University of Padova, Campus of Agripolis, mercial seed market, another one-third is provided by publicly Viale dell’Universita` 16, 35020 Legnaro, Italy funded institutions, and the seed saved by farmers accounts for the remainder. E. Albertini (&) Over the centuries, crop plants have followed the gen- Department of Applied Biology, University of Perugia, Borgo XX Giugno 74, 06121 Perugia, Italy eral pattern of introduction, selection, and hybridization. e-mail: [email protected] Crop introduction has been crucial for agriculture because 123 160 Plant Reprod (2013) 26:159–179 many of the world’s crops are produced outside their faster and cheaper (Fig. 1). The impact of apomictic crops region of domestication. Once introgressed, selection and in agriculture would be comparable to, or even greater breeding strategies have led to the development of new than, the impact of the Green Revolution, especially in cultivars with improved yield and adaptation. Plant Third World countries (Vielle-Calzada et al. 1996; Pupilli breeders are working to extend the Green Revolution by and Barcaccia 2012). In fact, it has been estimated that the intensifying selection, developing more hybrid varieties in use of apomixis technology in the production of hybrid rice more crops, and increasing the range of plant functions alone could provide benefits exceeding 1,800 million Eu- through mutation and transgenic breeding. Hence, plant ros per year (Spillane et al. 2004; Albertini et al. 2010). breeding will continue to play a crucial role in crop Apomixis technology could also provide benefits for improvement because the needs are many, the techniques clonally propagated crops. Clonal crop yields are limited are expanding, the new genetic combinations are limitless, by pathogens (mainly viral and endophytic), which accu- and the successes of the past illuminate the potential of the mulate over successive rounds of vegetative propagation future. In outcrossing species, alleles disseminate in the and seriously limit the yield and exchange of germplasms offspring; thus, the optimal genotype is lost together with between countries. The use of apomixis technology in these the desired trait. Exact copies of a superior genotype can be crops would provide the additional option and benefit of made via vegetative propagation; however, this technique propagation via clonal seeds and thus generating disease- is usually not applicable to annual crops such as maize, free material that can be more easily stored and trans- rice, and wheat. The fixation of a given genotype occurs ported. The use of apomictic seed as an alternative to naturally in species that exhibit an asexual type of seed vegetative propagules would provide similar benefits (e.g., production termed apomixis. This trait by itself is highly lower costs and higher yields) over the current use of true valuable for agriculture; however, despite many efforts, it seed of such crops. For example, apomixis technology has not been possible to introduce apomixis into modern could make true potato seeds a more attractive option for domesticated crop species. potato breeders and cultivators and would return benefits to As a reproductive strategy for cloning plants via seeds, growers of as much as 2.3 billion Euros per year (Spillane apomixis is a highly desirable trait in modern agriculture. et al. 2004). In fact, apomixis results in offspring that are exact genetic The development of apomixis technology in agriculture replices of the female parent because embryos are derived will require a deeper knowledge of the mechanisms regu- from the parthenogenic development of apomeiotic egg lating reproductive development in plants. Our molecular cells (for reviews on apomixis, see Bicknell and Koltunow understanding of apomixis would be greatly increased if 2004; Ozias-Akins 2006; Albertini et al. 2010; Pupilli and genes that are specifically or differentially expressed dur- Barcaccia 2012; Koltunow et al. 2013). From an evolu- ing the formation of the embryo and embryo sac could be tionary point of view, apomixis may be regarded as a identified. Over the last two decades, many scientists have consequence of sexual failure rather than as a recipe for speculated about the isolation of gene/s controlling key clonal success (Silvertown 2008). steps of the apomictic pathway, and many papers have Introgression of apomixis from wild relatives into crop postulated the production of engineered plants exhibiting species and transformation of sexual genotypes into apo- apomictic-like phenotypes. In fact, none of the major crop mictically reproducing genotypes are long-held goals of plants have been bred for apomixis, and only some features plant breeding. Breeders believe that the introduction of of apomixis have been genetically engineered in model apomixis into agronomically important crops will have species. Consequently, even in the era of genomics, revolutionary implications for agriculture. The potential achieving an understanding of the genetic control and benefits of harnessing apomixis are many and vary from molecular regulation of apomixis appears much more full exploitation of heterosis by reseeding the best hybrids complicated than expected. Large amounts of cytological to clonal propagation of the superior genotypes in seed- and ecological information, along with genetic and propagated outcrossing crops. The impact of apomictic molecular data, have been collected mainly from model crops in agriculture would be massive in both developed species (i.e., Boechera holboellii, Hieracium spp., Hyper- and developing countries. Unfortunately, barring a few icum perforatum, Paspalum spp., Poa pratensis, Ranun- exceptions in some forage grasses and fruit trees, apomixis culus spp., and Taraxacum officinale) and have often been is not a common feature among crop species. tested in Arabidopsis thaliana (Arabidopsis) to elucidate The fixation of hybrid vigor through apomixis is a the mechanisms of apomeiosis, parthenogenesis, and apo- desirable objective for breeders and farmers alike and is mixis. Several genes involved in the formation of unre- expected to have a revolutionary impact on food and duced embryo sacs and egg cells, in addition to genes agriculture production. The stabilization of heterozygous responsible for the autonomous development of the embryo genotypes via apomixis would make breeding programs and endosperm, have been cloned and characterized; 123 Plant Reprod (2013) 26:159–179
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