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3 pages, 165 KiB

Open AccessEditorial

Molecular Basis of Apomixis in Plants

by Diego Hojsgaard

Genes 2021, 12(4), 576; https://doi.org/10.3390/genes12040576 - 16 Apr 2021

Cited by 2 | Viewed by 2069

Abstract

Sexual reproduction in plants is a complex, stringently regulated process that leads to the creation of diaspores for a new generation: sexual seeds [...] Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

Research

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38 pages, 5553 KiB

Open AccessArticle

Whether Gametophytes Are Reduced or Unreduced in Angiosperms Might Be Determined Metabolically

by Mayelyn Mateo de Arias, Lei Gao, David A. Sherwood, Krishna K. Dwivedi, Bo J. Price, Michelle Jamison, Becky M. Kowallis and John G. Carman

Genes 2020, 11(12), 1449; https://doi.org/10.3390/genes11121449 - 02 Dec 2020

Cited by 13 | Viewed by 5010

Abstract

In angiosperms, meiotic failure coupled with the formation of genetically unreduced gametophytes in ovules (apomeiosis) constitute major components of gametophytic apomixis. These aberrant developmental events are generally thought to be caused by mutation. However, efforts to locate the responsible mutations have failed. Herein, [...] Read more.

In angiosperms, meiotic failure coupled with the formation of genetically unreduced gametophytes in ovules (apomeiosis) constitute major components of gametophytic apomixis. These aberrant developmental events are generally thought to be caused by mutation. However, efforts to locate the responsible mutations have failed. Herein, we tested a fundamentally different hypothesis: apomeiosis is a polyphenism of meiosis, with meiosis and apomeiosis being maintained by different states of metabolic homeostasis. Microarray analyses of ovules and pistils were used to differentiate meiotic from apomeiotic processes in Boechera (Brassicaceae). Genes associated with translation, cell division, epigenetic silencing, flowering, and meiosis characterized sexual Boechera (meiotic). In contrast, genes associated with stress responses, abscisic acid signaling, reactive oxygen species production, and stress attenuation mechanisms characterized apomictic Boechera (apomeiotic). We next tested whether these metabolic differences regulate reproductive mode. Apomeiosis switched to meiosis when premeiotic ovules of apomicts were cultured on media that increased oxidative stress. These treatments included drought, starvation, and H₂O₂ applications. In contrast, meiosis switched to apomeiosis when premeiotic pistils of sexual plants were cultured on media that relieved oxidative stress. These treatments included antioxidants, glucose, abscisic acid, fluridone, and 5-azacytidine. High-frequency apomeiosis was initiated in all sexual species tested: Brassicaceae, Boechera stricta, Boechera exilis, and Arabidopsis thaliana; Fabaceae, Vigna unguiculata; Asteraceae, Antennaria dioica. Unreduced gametophytes formed from ameiotic female and male sporocytes, first division restitution dyads, and nucellar cells. These results are consistent with modes of reproduction and types of apomixis, in natural apomicts, being regulated metabolically. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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15 pages, 1048 KiB

Open AccessArticle

Haploidy in Tobacco Induced by PsASGR-BBML Transgenes via Parthenogenesis

by Zhifen Zhang, Joann Conner, Yinping Guo and Peggy Ozias-Akins

Genes 2020, 11(9), 1072; https://doi.org/10.3390/genes11091072 - 12 Sep 2020

Cited by 24 | Viewed by 3005

Abstract

Background: Engineering apomixis in sexually reproducing plants has been long desired because of the potential to fix hybrid vigor. Validating the functionality of genes originated from apomictic species that contribute to apomixis upon transfer to sexually reproducing species is an important step. The [...] Read more.

Background: Engineering apomixis in sexually reproducing plants has been long desired because of the potential to fix hybrid vigor. Validating the functionality of genes originated from apomictic species that contribute to apomixis upon transfer to sexually reproducing species is an important step. The PsASGR-BABYBOOM-like (PsASGR-BBML) gene from Pennisetum squamulatum confers parthenogenesis in this apomict, and its functionality was demonstrated in several sexually reproducing monocots but not in any dicots. Methods: We introduced the PsASGR-BBML gene regulated by egg cell-specific promoters, either AtDD45 or AtRKD2, into tobacco, and analyzed progeny of the transgenic lines resulting from self-pollination and crossing by flow cytometry. Results: We identified haploid progeny at a frequency lower than 1% in the AtDD45_pro lines, while at a frequency of 9.3% for an octoploid (2n = 8x) AtRKD2_pro line. Haploid production in the T₂ generation, derived from the tetraploid T₁ offspring of this original octoploid AtRKD2_pro line, was also observed. Pollinated by homozygous transgenic tobacco carrying a DsRed marker gene, 4x progeny of the AtRKD2_pro line yielded parthenogenetic embryos identified as DsRed negative. We verified that the DsRed negative seedlings recovered were haploid (2x). Conclusion: The PsASGR-BBML gene regulated by egg cell-specific promoters could enable parthenogenesis in tobacco, a dicotyledon species. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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16 pages, 3958 KiB

Open AccessFeature PaperArticle

Efficient CRISPR/Cas9-Mediated Knockout of an Endogenous PHYTOENE DESATURASE Gene in T1 Progeny of Apomictic Hieracium Enables New Strategies for Apomixis Gene Identification

by Sam W. Henderson, Steven T. Henderson, Marc Goetz and Anna M. G. Koltunow

Genes 2020, 11(9), 1064; https://doi.org/10.3390/genes11091064 - 10 Sep 2020

Cited by 5 | Viewed by 4676

Abstract

Most Hieracium subgenus Pilosella species are self-incompatible. Some undergo facultative apomixis where most seeds form asexually with a maternal genotype. Most embryo sacs develop by mitosis, without meiosis and seeds form without fertilization. Apomixis is controlled by dominant loci where recombination is suppressed. [...] Read more.

Most Hieracium subgenus Pilosella species are self-incompatible. Some undergo facultative apomixis where most seeds form asexually with a maternal genotype. Most embryo sacs develop by mitosis, without meiosis and seeds form without fertilization. Apomixis is controlled by dominant loci where recombination is suppressed. Loci deletion by γ-irradiation results in reversion to sexual reproduction. Targeted mutagenesis of genes at identified loci would facilitate causal gene identification. In this study, the efficacy of CRISPR/Cas9 editing was examined in apomictic Hieracium by targeting mutations in the endogenous PHYTOENE DESATURASE (PDS) gene using Agrobacterium-mediated leaf disk transformation. In three experiments, the expected albino dwarf-lethal phenotype, characteristic of PDS knockout, was evident in 11% of T0 plants, 31.4% were sectorial albino chimeras, and the remainder were green. The chimeric plants flowered. Germinated T1 seeds derived from apomictic reproduction in two chimeric plants were phenotyped and sequenced to identify PDS gene edits. Up to 86% of seeds produced albino seedlings with complete PDS knockout. This was attributed to continuing Cas9-mediated editing in chimeric plants during apomictic seed formation preventing Cas9 segregation from the PDS target. This successful demonstration of efficient CRISPR/Cas9 gene editing in apomictic Hieracium, enabled development of the discussed strategies for future identification of causal apomixis genes. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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21 pages, 1988 KiB

Open AccessArticle

Genes Modulating the Increase in Sexuality in the Facultative Diplosporous Grass Eragrostis curvula under Water Stress Conditions

by Juan Pablo Selva, Diego Zappacosta, José Carballo, Juan Manuel Rodrigo, Andrés Bellido, Cristian Andrés Gallo, Jimena Gallardo and Viviana Echenique

Genes 2020, 11(9), 969; https://doi.org/10.3390/genes11090969 - 21 Aug 2020

Cited by 14 | Viewed by 2411

Abstract

Eragrostis curvula presents mainly facultative genotypes that reproduce by diplosporous apomixis, retaining a percentage of sexual pistils that increase under drought and other stressful situations, indicating that some regulators activated by stress could be affecting the apomixis/sexual switch. Water stress experiments were performed [...] Read more.

Eragrostis curvula presents mainly facultative genotypes that reproduce by diplosporous apomixis, retaining a percentage of sexual pistils that increase under drought and other stressful situations, indicating that some regulators activated by stress could be affecting the apomixis/sexual switch. Water stress experiments were performed in order to associate the increase in sexual embryo sacs with the differential expression of genes in a facultative apomictic cultivar using cytoembryology and RNA sequencing. The percentage of sexual embryo sacs increased from 4 to 24% and 501 out of the 201,011 transcripts were differentially expressed (DE) between control and stressed plants. DE transcripts were compared with previous transcriptomes where apomictic and sexual genotypes were contrasted. The results point as candidates to transcripts related to methylation, ubiquitination, hormone and signal transduction pathways, transcription regulation and cell wall biosynthesis, some acting as a general response to stress and some that are specific to the reproductive mode. We suggest that a DNA glycosylase EcROS1-like could be demethylating, thus de-repressing a gene or genes involved in the sexuality pathways. Many of the other DE transcripts could be part of a complex mechanism that regulates apomixis and sexuality in this grass, the ones in the intersection between control/stress and apo/sex being the strongest candidates. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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19 pages, 8720 KiB

Open AccessArticle

Genetic Dissection of Apomixis in Dandelions Identifies a Dominant Parthenogenesis Locus and Highlights the Complexity of Autonomous Endosperm Formation

by Peter J. Van Dijk, Rik Op den Camp and Stephen E. Schauer

Genes 2020, 11(9), 961; https://doi.org/10.3390/genes11090961 - 20 Aug 2020

Cited by 17 | Viewed by 4452

Abstract

Apomixis in the common dandelion (Taraxacum officinale) consists of three developmental components: diplospory (apomeiosis), parthenogenesis, and autonomous endosperm development. The genetic basis of diplospory, which is inherited as a single dominant factor, has been previously elucidated. To uncover the genetic basis [...] Read more.

Apomixis in the common dandelion (Taraxacum officinale) consists of three developmental components: diplospory (apomeiosis), parthenogenesis, and autonomous endosperm development. The genetic basis of diplospory, which is inherited as a single dominant factor, has been previously elucidated. To uncover the genetic basis of the remaining components, a cross between a diploid sexual seed parent and a triploid apomictic pollen donor was made. The resulting 95 triploid progeny plants were genotyped with co-dominant simple-sequence repeat (SSR) markers and phenotyped for apomixis as a whole and for the individual apomixis components using Nomarski Differential Interference Contrast (DIC) microscopy of cleared ovules and seed flow cytometry. From this, a new SSR marker allele was discovered that was closely linked to parthenogenesis and unlinked to diplospory. The segregation of apomixis as a whole does not differ significantly from a three-locus model, with diplospory and parthenogenesis segregating as unlinked dominant loci. Autonomous endosperm is regularly present without parthenogenesis, suggesting that the parthenogenesis locus does not also control endosperm formation. However, the high recovery of autonomous endosperm is inconsistent with this phenotype segregating as the third dominant locus. These results highlight the genetic complexity underlying apomixis in the dandelion and underline the challenge of introducing autonomous apomixis into sexual crops. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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24 pages, 4080 KiB

Open AccessArticle

The Role of APOSTART in Switching between Sexuality and Apomixis in Poa pratensis

by Gianpiero Marconi, Domenico Aiello, Bryan Kindiger, Loriano Storchi, Alessandro Marrone, Lara Reale, Niccolò Terzaroli and Emidio Albertini

Genes 2020, 11(8), 941; https://doi.org/10.3390/genes11080941 - 14 Aug 2020

Cited by 8 | Viewed by 3789

Abstract

The production of seeds without sex is considered the holy grail of plant biology. The transfer of apomixis to various crop species has the potential to transform plant breeding, since it will allow new varieties to retain valuable traits thorough asexual reproduction. Therefore, [...] Read more.

The production of seeds without sex is considered the holy grail of plant biology. The transfer of apomixis to various crop species has the potential to transform plant breeding, since it will allow new varieties to retain valuable traits thorough asexual reproduction. Therefore, a greater molecular understanding of apomixis is fundamental. In a previous work we identified a gene, namely APOSTART, that seemed to be involved in this asexual mode of reproduction, which is very common in Poa pratensis L., and here we present a detailed work aimed at clarifying its role in apomixis. In situ hybridization showed that PpAPOSTART is expressed in reproductive tissues from pre-meiosis to embryo development. Interestingly, it is expressed early in few nucellar cells of apomictic individuals possibly switching from a somatic to a reproductive cell as in aposporic apomixis. Moreover, out of 13 APOSTART members, we identified one, APOSTART_6, as specifically expressed in flower tissue. APOSTART_6 also exhibited delayed expression in apomictic genotypes when compared with sexual types. Most importantly, the SCAR (Sequence Characterized Amplified Region) derived from the APOSTART_6 sequence completely co-segregated with apomixis. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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22 pages, 1632 KiB

Open AccessArticle

Chasing the Apomictic Factors in the Ranunculus auricomus Complex: Exploring Gene Expression Patterns in Microdissected Sexual and Apomictic Ovules

by Marco Pellino, Diego Hojsgaard, Elvira Hörandl and Timothy F. Sharbel

Genes 2020, 11(7), 728; https://doi.org/10.3390/genes11070728 - 30 Jun 2020

Cited by 13 | Viewed by 2615

Abstract

Apomixis, the asexual reproduction via seeds, is associated to polyploidy and hybridization. To identify possible signatures of apomixis, and possible candidate genes underlying the shift from sex to apomixis, microarray-based gene expression patterns of live microdissected ovules at four different developmental stages were [...] Read more.

Apomixis, the asexual reproduction via seeds, is associated to polyploidy and hybridization. To identify possible signatures of apomixis, and possible candidate genes underlying the shift from sex to apomixis, microarray-based gene expression patterns of live microdissected ovules at four different developmental stages were compared between apomictic and sexual individuals of the Ranunculus auricomus complex. Following predictions from previous work on mechanisms underlying apomixis penetrance and expressivity in the genus, gene expression patterns were classified into three categories based on their relative expression in apomicts compared to their sexual parental ancestors. We found evidence of misregulation and differential gene expression between apomicts and sexuals, with the highest number of differences detected during meiosis progression and emergence of aposporous initial (AI) cells, a key developmental stage in the ovule of apomicts where a decision between divergent reproductive pathways takes place. While most of the differentially expressed genes (DEGs) could not be annotated, gene expression was classified into transgressive, parent of origin and ploidy effects. Genes related to gametogenesis and meiosis demonstrated patterns reflective of transgressive and genome dosage effects, which support the hypothesis of a dominant factor controlling apomixis in Ranunculus and modulated by secondary modifiers. Three genes with probable functions in sporogenesis and gametogenesis development are identified and characterized for future studies. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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Review

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27 pages, 5808 KiB

Open AccessReview

How to Become an Apomixis Model: The Multifaceted Case of Paspalum

by Juan Pablo A. Ortiz, Fulvio Pupilli, Carlos A. Acuña, Olivier Leblanc and Silvina C. Pessino

Genes 2020, 11(9), 974; https://doi.org/10.3390/genes11090974 - 21 Aug 2020

Cited by 15 | Viewed by 3431

Abstract

In the past decades, the grasses of the Paspalum genus have emerged as a versatile model allowing evolutionary, genetic, molecular, and developmental studies on apomixis as well as successful breeding applications. The rise of such an archetypal system progressed through integrative phases, which [...] Read more.

In the past decades, the grasses of the Paspalum genus have emerged as a versatile model allowing evolutionary, genetic, molecular, and developmental studies on apomixis as well as successful breeding applications. The rise of such an archetypal system progressed through integrative phases, which were essential to draw conclusions based on solid standards. Here, we review the steps adopted in Paspalum to establish the current body of knowledge on apomixis and provide model breeding programs for other agronomically important apomictic crops. In particular, we discuss the need for previous detailed cytoembryological and cytogenetic germplasm characterization; the establishment of sexual and apomictic materials of identical ploidy level; the development of segregating populations useful for inheritance analysis, positional mapping, and epigenetic control studies; the development of omics data resources; the identification of key molecular pathways via comparative gene expression studies; the accurate molecular characterization of genomic loci governing apomixis; the in-depth functional analysis of selected candidate genes in apomictic and model species; the successful building of a sexual/apomictic combined breeding scheme. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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20 pages, 1474 KiB

Open AccessReview

A Reappraisal of the Evolutionary and Developmental Pathway of Apomixis and Its Genetic Control in Angiosperms

by Gianni Barcaccia, Fabio Palumbo, Sergio Sgorbati, Emidio Albertini and Fulvio Pupilli

Genes 2020, 11(8), 859; https://doi.org/10.3390/genes11080859 - 28 Jul 2020

Cited by 15 | Viewed by 3894

Abstract

Apomixis sensu stricto (agamospermy) is asexual reproduction by seed. In angiosperms it represents an easy byway of life cycle renewal through gamete-like cells that give rise to maternal embryos without ploidy reduction (meiosis) and ploidy restitution (syngamy). The origin of apomixis still represents [...] Read more.

Apomixis sensu stricto (agamospermy) is asexual reproduction by seed. In angiosperms it represents an easy byway of life cycle renewal through gamete-like cells that give rise to maternal embryos without ploidy reduction (meiosis) and ploidy restitution (syngamy). The origin of apomixis still represents an unsolved problem, as it may be either evolved from sex or the other way around. This review deals with a reappraisal of the origin of apomixis in order to deepen knowledge on such asexual mode of reproduction which seems mainly lacking in the most basal angiosperm orders (i.e., Amborellales, Nymphaeales and Austrobaileyales, also known as ANA-grade), while it clearly occurs in different forms and variants in many unrelated families of monocots and eudicots. Overall findings strengthen the hypothesis that apomixis as a whole may have evolved multiple times in angiosperm evolution following different developmental pathways deviating to different extents from sexuality. Recent developments on the genetic control of apomixis in model species are also presented and adequately discussed in order to shed additional light on the antagonist theories of gain- and loss-of-function over sexuality. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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29 pages, 1115 KiB

Open AccessEditor’s ChoiceReview

Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation

by Anja Schmidt

Genes 2020, 11(3), 329; https://doi.org/10.3390/genes11030329 - 20 Mar 2020

Cited by 50 | Viewed by 8760

Abstract

In higher plants, sexual and asexual reproduction through seeds (apomixis) have evolved as alternative strategies. As apomixis leads to the formation of clonal offspring, its great potential for agricultural applications has long been recognized. However, the genetic basis and the molecular control underlying [...] Read more.

In higher plants, sexual and asexual reproduction through seeds (apomixis) have evolved as alternative strategies. As apomixis leads to the formation of clonal offspring, its great potential for agricultural applications has long been recognized. However, the genetic basis and the molecular control underlying apomixis and its evolutionary origin are to date not fully understood. Both in sexual and apomictic plants, reproduction is tightly controlled by versatile mechanisms regulating gene expression, translation, and protein abundance and activity. Increasing evidence suggests that interrelated pathways including epigenetic regulation, cell-cycle control, hormonal pathways, and signal transduction processes are relevant for apomixis. Additional molecular mechanisms are being identified that involve the activity of DNA- and RNA-binding proteins, such as RNA helicases which are increasingly recognized as important regulators of reproduction. Together with other factors including non-coding RNAs, their association with ribosomes is likely to be relevant for the formation and specification of the apomictic reproductive lineage. Subsequent seed formation appears to involve an interplay of transcriptional activation and repression of developmental programs by epigenetic regulatory mechanisms. In this review, insights into the genetic basis and molecular control of apomixis are presented, also taking into account potential relations to environmental stress, and considering aspects of evolution. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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Other

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28 pages, 2647 KiB

Open AccessDiscussion

Can We Use Gene-Editing to Induce Apomixis in Sexual Plants?

by Armin Scheben and Diego Hojsgaard

Genes 2020, 11(7), 781; https://doi.org/10.3390/genes11070781 - 12 Jul 2020

Cited by 14 | Viewed by 5637

Abstract

Apomixis, the asexual formation of seeds, is a potentially valuable agricultural trait. Inducing apomixis in sexual crop plants would, for example, allow breeders to fix heterosis in hybrid seeds and rapidly generate doubled haploid crop lines. Molecular models explain the emergence of functional [...] Read more.

Apomixis, the asexual formation of seeds, is a potentially valuable agricultural trait. Inducing apomixis in sexual crop plants would, for example, allow breeders to fix heterosis in hybrid seeds and rapidly generate doubled haploid crop lines. Molecular models explain the emergence of functional apomixis, i.e., apomeiosis + parthenogenesis + endosperm development, as resulting from a combination of genetic or epigenetic changes that coordinate altered molecular and developmental steps to form clonal seeds. Apomixis-like features and synthetic clonal seeds have been induced with limited success in the sexual plants rice and maize by using gene editing to mutate genes related to meiosis and fertility or via egg-cell specific expression of embryogenesis genes. Inducing functional apomixis and increasing the penetrance of apomictic seed production will be important for commercial deployment of the trait. Optimizing the induction of apomixis with gene editing strategies that use known targets as well as identifying alternative targets will be possible by better understanding natural genetic variation in apomictic species. With the growing availability of genomic data and precise gene editing tools, we are making substantial progress towards engineering apomictic crops. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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24 pages, 995 KiB

Open AccessOpinion

Apomixis Technology: Separating the Wheat from the Chaff

by Diego Hojsgaard

Genes 2020, 11(4), 411; https://doi.org/10.3390/genes11040411 - 10 Apr 2020

Cited by 24 | Viewed by 5677

Abstract

Projections indicate that current plant breeding approaches will be unable to incorporate the global crop yields needed to deliver global food security. Apomixis is a disruptive innovation by which a plant produces clonal seeds capturing heterosis and gene combinations of elite phenotypes. Introducing [...] Read more.

Projections indicate that current plant breeding approaches will be unable to incorporate the global crop yields needed to deliver global food security. Apomixis is a disruptive innovation by which a plant produces clonal seeds capturing heterosis and gene combinations of elite phenotypes. Introducing apomixis into hybrid cultivars is a game-changing development in the current plant breeding paradigm that will accelerate the generation of high-yield cultivars. However, apomixis is a developmentally complex and genetically multifaceted trait. The central problem behind current constraints to apomixis breeding is that the genomic configuration and molecular mechanism that initiate apomixis and guide the formation of a clonal seed are still unknown. Today, not a single explanation about the origin of apomixis offer full empirical coverage, and synthesizing apomixis by manipulating individual genes has failed or produced little success. Overall evidence suggests apomixis arise from a still unknown single event molecular mechanism with multigenic effects. Disentangling the genomic basis and complex genetics behind the emergence of apomixis in plants will require the use of novel experimental approaches benefiting from Next Generation Sequencing technologies and targeting not only reproductive genes, but also the epigenetic and genomic configurations associated with reproductive phenotypes in homoploid sexual and apomictic carriers. A comprehensive picture of most regulatory changes guiding apomixis emergence will be central for successfully installing apomixis into the target species by exploiting genetic modification techniques. Full article

(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

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