Akagi, T.

Pilkington, S. M.

Testolin, R.

Frontiers in Plant Science

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PubMed

Raffaele Testolin

Sarah M. Pilkington

Takashi Akagi

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Editorial: Dioecy in Fruit Crops: The Gender Rise and Decline and Its Agronomic Impact

Testolin R.

Pilkington S. M.

Akagi T.

Archivio istituzionale della ricerca - Università degli Studi di Udine

EDITORIALpublished: 15 July 2021doi: 10.3389/fpls.2021.719588Frontiers in Plant Science | www.frontiersin.org 1 July 2021 | Volume 12 | Article 719588Edited and reviewed by:Michael Nicolas,Centro Nacional de Biotecnología,Consejo Superior de InvestigacionesCientíficas (CSIC), Spain*Correspondence:Raffaele Testolinraffaele.testolin@uniud.itSpecialty section:This article was submitted toPlant Development and EvoDevo,a section of the journalFrontiers in Plant ScienceReceived: 02 June 2021Accepted: 14 June 2021Published: 15 July 2021Citation:Testolin R, Pilkington SM and Akagi T(2021) Editorial: Dioecy in Fruit Crops:The Gender Rise and Decline and ItsAgronomic Impact.Front. Plant Sci. 12:719588.doi: 10.3389/fpls.2021.719588Editorial: Dioecy in Fruit Crops: TheGender Rise and Decline and ItsAgronomic ImpactRaffaele Testolin 1*, Sarah M. Pilkington 2 and Takashi Akagi 31Department of Agricultural, Food, Animal and Environmental Sciences, University of Udine, Udine, Italy, 2 Plant & FoodResearch, The New Zealand Institute for Plant and Food Research Ltd., Auckland, New Zealand, 3Graduate School ofEnvironmental and Life Science, Okayama University, Okayama, JapanKeywords: dioecious crops, sex determination, sex chromosomes, dioecy evolution, sex transitionEditorial on the Research TopicDioecy in Fruit Crops: The Gender Rise and Decline and Its Agronomic ImpactSexuality in animals is a rather stable trait, with the male genetic determinant operating in a femalebackground, but is more complex in flowering plants.Hermaphroditism (perfect flowers with both sexes expressed) is recognized as being the mostancient state in the evolution of Angiosperms. It has evolved into monoecism (separated sexes inthe same individual) and gymnodioecism (individuals carrying only female flowers), which in turnhas evolved to dioecism (male and female sexes in different individuals). These transitions couldhave occurred many times, with reversion to hermaphroditism occurring frequently as well.This complex and unstable sexuality of plants has attracted the interest of scientists since 1,715when Sébastien Vaillant, botanist at the “Jardin Royal des Plantes médicinales” (now “Le Jardin desPlantes”) in Paris, hypothesized the occurrence of sexual dimorphism in pistachio (Pistacia vera).Dioecy occurs in 5–6% of flowering plants but could reach 20% among the crop species and istherefore of economic interest, prompting this Frontiers Research Topic.The Research Topic was launched in July 2019 and collected 115 potential contributors, mostof which became irresponsive after the spread of Sars-Cov-2 pandemic. However, we are happy, aseditors, to have collected two excellent reviews and original papers on persimmon (Diospyros) anddate palm (Phoenix).In short, Montalvão et al. offer an exhaustive view of the diversity and dynamics of sexdetermination in plants. The authors describe in their report that dioecy was found in some15,600 species, spread over 175 families and 987 genera and suggest that the evolution took placeindependently hundreds, if not thousands, of times. With the control of gender being ratherunstable, the reversion from dioecy to hermaphroditism might have occurred frequently as well.Indeed, two mutations or even a single mutation could drive the reversion.The key message that emerges from this well-documented review is that while the formalgenetic model—the “two-genes model”—first postulated by MogensWestergard in 1958 and bettershaped by Brian and Deborah Charlesworth later on, remains substantially true, the molecularinvestigation of the recent years would suggest that the genes involved are not always the same.The scientists list 25 different genes involved in dioecy, either to suppress femaleness or to promotemaleness. What is clearly emerging is that different genes are involved in the same pathway andproduce analogous phenotypic mutations. This is the case, for instance, for the nine genes involvedin the cytokinin signaling, a key plant hormone, the level of which determines the gynoeciumformation. Similarly, five different genes are involved in the micro-sporogenesis process that occursin the tapetum and leads to the release of fertile pollen in male individuals.Testolin et al. Editorial: Dioecy in Fruit Crops. The Gender Rise and DeclineSuppressors and promoters are connected either through agenetic linkage in the sex-determining region (SDR), whererecombination between the sex-determinants is suppressed,or through an epistatic genetic interaction, that would notrequire linkage.Indeed, dioecy might have developed from hermaphroditismthrough the intermediate step of gynodioeciousness (femaleindividuals, where the pollen development is arrested) or throughmonoecy. The evolution of dioecy from monoecy would requirea single gene that determines the sexual orientation, independentof the number of genes that control the development of stamensand carpels.This aspect of dioecy has been revised for this ResearchTopic by Cronk and Müller, who analyzed species like Diospyros,Populus, and Salix. The authors point out that the separationof unisexual flowers has already occurred in the monoeciousancestor; therefore, the evolution toward dioecy may be a simplematter of separating pre-existing epistatic regulatory architectureto different individuals, which may be accomplished by a singlemaster regulator gene (the ARR17 gene for Populus and theMeGI gene forDiospyros), either in a hemizygous state or toggledon–off by a suppressor (YARR17-IR and OGI, respectively, forPopulus and Diospyros).The Research Topic includes two valuable papers onpersimmon and date palm. The first of two was preceded in theliterature by several papers of the same authors on the complex,and in some instances incomplete, dioecy of this crop; while thesecond one introduces for the first time a molecular analysis ofthe SDR in Phoenix.The contribution from Masuda et al. provides a deep insightintoDiospyros, a genus that contains around 450 different speciesall dioecious or sub-dioecious and is becoming a model forthe study of the fine tuning of sex expression. The authorsfocused on a transition out of dioecy into monoecy in hexaploidDiospyros kaki (Oriental persimmon), which is based on theirprevious study for epigenetic silencing of the sex determinants,OGI and MeGI. They studied a cultivar with high-frequent maleflowers, uncovering the mechanism by which the epigeneticsilencing of MeGI/OGI is regulated. The male-rich cultivarshowed strong DNAmethylation in the OGI promoter, as well asin other female-rich cultivars, while OGI expression in the male-rich cultivar is released from silencing. Further transcriptomicapproaches suggested gene networks relating stress- or jasmonatesignal might involve the release of OGI silencing via chromatinremodeling or histone-methylations. Masuda et al. provided aninsight into themolecularmechanism to generate a well-balancedmonoecious system evolved from dioecy.The last paper included in this Research Topic on dioecy isfrom Torres et al. who reported updated information on datepalm (Phoenix dactylifera), the most recent species on whichthe gender control has been explored at the molecular level. Indate palm, there is the classical X/Y chromosome system, but theevolution of the Y chromosome, in absence of recombination, hasled to a large-scale re-arrangement of the sex-determining region,detected by the analysis of the density of k-mers in the assembledscaffolds of the SDR region sequenced in three different malegenotypes. The degeneration of the non-recombining Y-regionis known among the evolutionists as the “Muller’s ratchet”,according to which the lack of recombination (the “ratchet”)forces the degeneration of the region. Torres et al. provideexperimental evidence of this evolutionary mechanism.AUTHOR CONTRIBUTIONSAll authors listed have made a substantial, direct and intellectualcontribution to the work, and approved it for publication.Conflict of Interest: The authors declare that the research was conducted in theabsence of any commercial or financial relationships that could be construed as apotential conflict of interest.Copyright © 2021 Testolin, Pilkington and Akagi. This is an open-access articledistributed under the terms of the Creative Commons Attribution License (CC BY).The use, distribution or reproduction in other forums is permitted, provided theoriginal author(s) and the copyright owner(s) are credited and that the originalpublication in this journal is cited, in accordance with accepted academic practice.No use, distribution or reproduction is permitted which does not comply with theseterms.Frontiers in Plant Science | www.frontiersin.org 2 July 2021 | Volume 12 | Article 719588

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Editorial: Dioecy in Fruit Crops: The Gender Rise and Decline and Its Agronomic Impact

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