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Plant Sex Chromosome Evolution

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Plant Sex Chromosome Evolution Journal of Experimental Botany Advance Access published November 3, 2012 Journal of Experimental Botany , Vol. 63, No. 2, pp. 695–709, 2012 doi:10.1093/jxb/err313doi:10.1093/jxb/ers322 Advance Access publication 4 November, 2011 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) RESEARCHFLOWERING PAPER NEWSLETTER REVIEW InPlantPosidonia sex chromosome oceanica cadmium evolution induces changes in DNA methylation and chromatin patterning Deborah Charlesworth* MariaInstituteGreco, of Evolutionary Adriana Biology, Chiappetta, School of LeonardoBiological Sciences, Bruno andThe University Maria Beatrice of Edinburgh, Bitonti* The King’s Buildings, West Mains Road, Edinburgh EH9 3JT, UK Department of Ecology, University of Calabria, Laboratory of Plant Cyto-physiology, Ponte Pietro Bucci, I-87036 Arcavacata di Rende, Cosenza,* To whom Italy correspondence should be addressed. E-mail: [email protected] Downloaded from * To whom correspondence should be addressed. E-mail: [email protected] Received 15 August 2012; Revised 16 October 2012; Accepted 17 October 2012 Received 29 May 2011; Revised 8 July 2011; Accepted 18 August 2011 Abstract http://jxb.oxfordjournals.org/ AbstractIt is now well established that plants have an important place in studies of sex chromosome evolution because of Inthe mammals, repeated cadmiumindependent is widely evolution considered of separate as a sexes non-genotoxic and sex chromosomes. carcinogen acting There through has been a methylation-dependent considerable recent epigeneticprogress in mechanism. studying plant Here, sex the chromosomes. effects of Cd In treatment this review, on theI focus DNA on methylation how these pattenrecent arestudies examined have helped together clarify with itsor answer effect on several chromatin important reconfiguration questions inaboutPosidonia sex chromosome oceanica. DNA evolution, methylation and I shall level andalso patterntry to clarify were some analysed com in- activelymon misconceptions. growing organs, I also under outline short- future (6 h) work and long-that will (2 dbe or needed 4 d) term to andmake low further (10 m M)progress, and high including (50 mM) testing doses ofsome Cd, throughimportant a ideas Methylation-Sensitive by genetic, molecular, Amplification and developmental Polymorphism approaches. technique Systems and with an immunocytologicaldifferent ages can clearly approach, help show the time course of events during changes from an ancestral co-sexual state (hermaphroditism or monoecy), respectively. The expression of one member of the CHROMOMETHYLASE (CMT) family, a DNA methyltransferase, at University of Georgia Libraries on October 22, 2014 wasand I will also also assessed explain byhow qRT-PCR. different questions Nuclear chromatin can be studied ultrastructure in lineages was whose investigated dioecy or sex by chromosomes transmission electronevolved microscopy.at different times Cd treatment in the past. induced a DNA hypermethylation, as well as an up-regulation of CMT, indicating that de novo methylation did indeed occur. Moreover, a high dose of Cd led to a progressive heterochromatinization of interphaseKey words: nucleiHermaphrodite, and apoptotic papaya, figures recombination were also suppression, observed afterSilene long-term, transposable treatment. element, The Y chromosome. data demonstrate that Cd perturbs the DNA methylation status through the involvement of a specific methyltransferase. Such changes are linked to nuclear chromatin reconfiguration likely to establish a new balance of expressed/repressed chromatin. Overall, the data show an epigenetic basis to the mechanism underlying Cd toxicity in plants. Introduction: the evolution of separate Keysexes words: and5-Methylcytosine-antibody, sex chromosomes cadmium-stress condition, chromatin reconfiguration, CHROMOMETHYLASE, DNA-methylation, Methylation- Sensitive Amplification Polymorphism (MSAP), Posidonia oceanica (L.) Delile. The study of plant sex chromosome involves non-model in understanding such strange phenomena has led to studies organisms, and the results have no obvious immediate applied in a diversity of dioecious plants, even though separate sexes benefits for crops in most countries, apart from the useful- are rare among flowering plants, and sex chromosomes are Introductionness of genetic markers for sexing plants before flowering, so not present in all dioecious plants, though they are common as to increase the proportion of females (the desired sex for in liverworts (Westergaard, 1958; Renner and Ricklefs, 1995; Infruit the crops Mediterranean such as grapevines, coastal kiwi ecosystem, fruit, date thepalms, endemic hops, MingAlthough et al., 2011 not). essential As will be for explained plant growth, below, plants in terrestrial appear seagrassholly trees,Posidonia strawberries, oceanica and (L.)Cannabis Delile sativa plays), aor relevant of males role in plants,to have Cdsex-determining is readily absorbed systems by of roots different and ages, translocated whereas into the byasparagus ensuring or primarypapaya (where production, a hermaphroditic water oxygenation form of male and aerialbest studied organs animal while, insystems, acquatic in mammals, plants, it is birds, directly and taken insects, up providesthat fruits niches well is foroften some desired). animals, Nevertheless, besides counteractingthere is wide byare leaves.ancient. In Thus plants, plants Cd absorptioncan be used induces to study complex the time changes course coastalinterest erosionin understanding through its sex widespread chromosome meadows evolution, (Ott, which 1980; atof events the genetic, during biochemicalsex chromosome and physiologicalevolution. levels which Piazziinvolveset strange al., 1999; phenomena Alcoverro suchet as al. selection, 2001). for There suppression is also ultimatelyAs will become account clear, for its understanding toxicity (Valle the and evolution Ulmer, of 1972; sex considerableof genetic recombination evidence that (whichP. oceanica is widespreadplants arethroughout able to Sanitchromosomesdi Toppi is andimpossible Gabrielli, without 1999; first Benavides understandinget al., 2005; the z absorbthe genomes and of accumulate most organisms, metals other from than sediments in parts (Sanchiz of the Weberevolutionet of al. ,separate 2006; Liu sexes,et al.because, 2008). the The genetic most changes obvious etsex al. chromosomes),, 1990; Pergent-Martini, and the resulting 1998; Maserti ‘geneticet al.degeneration’, 2005) thus symptominvolved in of the Cd latter toxicity lead is awith reduction high probability in plant growth to the due chro to- influencinginvolving loss metal of function, bioavailability or complete in the loss, marine of many ecosystem. genes on anmosomes inhibition involved of photosynthesis, losing recombination, respiration, and andit is nitrogenloss of Forthe non-recombining this reason, this chromosome; seagrass is widely this chromosome considered tois the be metabolism,recombination as that well leads as to a reductionthe special inproperties water and of sex mineral chro- aY metalin XY bioindicatorsystems, and speciesthe W in (Maserti ZW systemset al. ,such 1988; as Pergentthat of uptakemosomes. (Ouzonidou Studies ofet species al., 1997; that Perfus-Barbeoch have recently evolvedet al., 2000;sepa- etbirds al. and, 1995; Lepidoptera, Lafabrie andet a al. few, 2007). plants. CdThe isintrinsic one of interest most Shuklarate sexeset are al., ideal 2003; for Sobkowiak testing the and idea Deckert, that hermaphrodites 2003). are widespread heavy metals in both terrestrial and marine At the genetic level, in both animals and plants, Cd environments. can induce chromosomal aberrations, abnormalities in ª© 2011The Author The Author(s). [2012]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. ThisFor permissions, is an Open Access please articleemail: [email protected] under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Page 2 of 16 | Charlesworth selected to ‘compromise’ between male and female functions, Genetic and environmental control of plant an important test case for the existence of trade-offs between sex determination different functions. If this idea is correct, then changing from being hermaphrodite to becoming purely female or male Even restricting the term ‘sex’ to mean the gender of indi- ought to trigger a burst of adaptation, as females optimize viduals, the terminology of plant sex types is still confusing, their female functions, and males optimize their male func- and some definitions are needed. The term ‘unisexuality’ tions. Testing for such adaptive changes on sex chromosomes, applies to several distinct situations observed in plants, cov- and testing whether they are involved in recombination sup- ering species with environmental sex determination (e.g. pression between Y and X chromosomes, therefore has wide Policansky, 1981; Zimmerman, 1991; Pannell, 1997a) and implications. monoecious species, as well as dioecious species. Here, I shall use ‘sex-determining gene’ only for dioecious species with genetic sex determination. In monoecious species and in envi- Sexes and mating types ronmental sex determination, genes are,
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