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Multiple Photosynthetic Transitions, Polyploidy, and Lateral Gene Transfer in the Grass Subtribe Neurachninae

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Multiple Photosynthetic Transitions, Polyploidy, and Lateral Gene Transfer in the Grass Subtribe Neurachninae Journal of Experimental Botany , Vol. 63, 63, No. No. 17, 2, pp. pp. 695–709, 6297–6308, 2012 2012 doi:10.1093/jxb/err313doi:10.1093/jxb/ers282 Advance Access publication 4 November, 2011 This paper is available online free of of all all access access charges charges (see (see http://jxb.oxfordjournals.org/open_access.html http://jxb.oxfordjournals.org/open_access.html for for further further details) details) RESEARCHRESEARCH PAPERPAPER InMultiplePosidonia photosynthetic oceanica cadmium transitions, induces polyploidy, changes and in lateral DNA methylationgene transfer and in the chromatin grass subtribe patterning Neurachninae MariaPascal-Antoine Christin Greco, Adriana Chiappetta,1, Mark J. Wallace Leonardo2,3, BrunoHarmony Clayton and Maria Beatrice4, Erika J. Edwards Bitonti* 1, Robert T. Furbank5, Paul 4 6 7 4, DepartmentW. Hattersley of Ecology,, Rowan University F. Sage of Calabria,, Terry D. Macfarlane Laboratory of Plant and Cyto-physiology, Martha Ludwig Ponte* Pietro Bucci, I-87036 Arcavacata di Rende, Cosenza,1 Department Italy of Ecology and Evolutionary Biology, Brown University, 80 Waterman St., Providence, RI 02912, USA *2 ToSchool whom of correspondencePlant Biology, University should beof Western addressed. Australia, E-mail: Crawley, [email protected] WA 6009, Australia 3 Botanic Gardens and Parks Authority, Kings Park and Botanic Garden, West Perth, WA 6005, Australia 4 School of Chemistry and Biochemistry, University of Western Australia, Crawley, WA 6009, Australia Received 29 May 2011; Revised 8 July 2011; Accepted 18 August 2011 Downloaded from 5 CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia 6 Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S3B2, Canada Abstract7 Western Australian Herbarium, Science Division, Department of Environment & Conservation, Locked Bag 2, Manjimup, WA 6258, Australia In mammals, cadmium is widely considered as a non-genotoxic carcinogen acting through a methylation-dependent epigenetic* To whom correspondence mechanism. Here,should the be addressed. effects of E-mail: Cd treatment [email protected] on the DNA methylation patten are examined together with http://jxb.oxfordjournals.org/ its effect on chromatin reconfiguration in Posidonia oceanica. DNA methylation level and pattern were analysed in activelyReceived 6 growing July 2012; organs, Revised under6 September short- 2012; (6 h) Accepted and long- 18 September (2 d or 4 d)2012 term and low (10 mM) and high (50 mM) doses of Cd, through a Methylation-Sensitive Amplification Polymorphism technique and an immunocytological approach, respectively. The expression of one member of the CHROMOMETHYLASE (CMT) family, a DNA methyltransferase, wasAbstract also assessed by qRT-PCR. Nuclear chromatin ultrastructure was investigated by transmission electron microscopy. Cd treatment induced a DNA hypermethylation, as well as an up-regulation of CMT, indicating that de novoThe Neurachninaemethylation didis the indeed only occur.grass lineage Moreover, known a high to contain dose of C Cd3, C led4, and to C a3–C progressive4 intermediate heterochromatinization species, and as such of at Brown University on January 24, 2013 interphasehas been suggested nuclei and as apoptotic a model figuressystem were for studies also observed of photosynthetic after long-term pathway treatment. evolution The in data the Poaceae; demonstrate however, that Cd a perturbslack of a robust the DNA phylogenetic methylation framework status through has hindered the involvement this possibility. of a specificIn this study, methyltransferase. plastid and nuclear Such markers changes were are linkedused to to reconstruct nuclear chromatin evolutionary reconfiguration relationships likely among to Neurachninae establish a new species. balance In addition, of expressed/repressed photosynthetic types chromatin. were Overall,determined the datawith showcarbon an isotope epigenetic ratios, basis and to genome the mechanism sizes with underlying flow cytometry. Cd toxicity A high in plants. frequency of autopolyploidy was found in the Neurachninae, including in Neurachne munroi F.Muell. and Paraneurachne muelleri S.T.Blake, which Keyindependently words: 5-Methylcytosine-antibody, evolved C4 photosynthesis. cadmium-stress Phylogenetic condition, analyses chromatin also showed reconfiguration, that followingCHROMOMETHYLASE their separate C,4 origins, DNA-methylation,these two taxa exchanged Methylation- aSensitive gene encoding Amplification the C Polymorphism4 form of phospho (MSAP),enolPosidoniapyruvate oceanica carboxylase.(L.) Delile. The C3–C4 intermedi- ate Neurachne minor S.T.Blake is phylogenetically distinct from the two C4 lineages, indicating that intermediacy in this species evolved separately from transitional stages preceding C4 origins. The Neurachninae shows a substantial capacity to evolve new photosynthetic pathways repeatedly. Enablers of these transitions might include anatomical Introductionpre-conditions in the C3 ancestor, and frequent autopolyploidization. Transfer of key C4 genetic elements between independently evolved C4 taxa may have also facilitated a rapid adaptation of photosynthesis in these grasses that Inhad theto survive Mediterranean in the harsh coastal climate ecosystem, appearing the during endemic the late PlioceneAlthough in notAustralia. essential for plant growth, in terrestrial seagrass Posidonia oceanica (L.) Delile plays a relevant role plants, Cd is readily absorbed by roots and translocated into byKeywords: ensuring C primary4 grass evolution, production, C4 photosynthesis, water oxygenation C3–C4 intermediate, and aerial grass organs phylogeny, while, in acquaticlateral gene plants, transfer, it is Neurachne directly taken, up providesParaneurachne niches, polyploidy for some animals, besides counteracting by leaves. In plants, Cd absorption induces complex changes coastal erosion through its widespread meadows (Ott, 1980; at the genetic, biochemical and physiological levels which Piazzi et al., 1999; Alcoverro et al., 2001). There is also ultimately account for its toxicity (Valle and Ulmer, 1972; considerable evidence that P. oceanica plants are able to Sanit di Toppi and Gabrielli, 1999; Benavides et al., 2005; z absorbIntroduction and accumulate metals from sediments (Sanchiz Weber et al., 2006; Liu et al., 2008). The most obvious et al., 1990; Pergent-Martini, 1998; Maserti et al., 2005) thus symptom of Cd toxicity is a reduction in plant growth due to influencingDespite its metalcomplexity, bioavailability the C4 photosynthetic in the marine pathway ecosystem. has anC4 lineages inhibition have of been photosynthesis, postulated in the respiration, PACMAD and clade nitrogen (Grass Forevolved this independently reason, this >62 seagrass times in is flowering widely considered plants (Sage toet al be., metabolism,Phylogeny Working as well Group as a II, reduction 2012). Such in a waterclustering and of mineral C4 ori- a2011 metal), thus bioindicator constitutingspecies a striking (Maserti exampleet of al. convergent, 1988; Pergent evolu- uptakegins is also (Ouzonidou observedet in al.other, 1997; groups, Perfus-Barbeoch with six independentet al., 2000; lin- ettion. al. It, is 1995; especially Lafabrie prevalentet al. in, grasses, 2007). Cdwhere is 22–24 one of distinct most Shuklaeages inet the al. sedges, 2003; (Cyperaceae) Sobkowiak and and Deckert, 23 in the 2003). Caryophyllales 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 © 2012 The Author(s). ªThis2011 is an The Open Author(s). Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ Thisby-nc/2.0/uk/ is an Open) which Access permits article unrestricted distributed non-commercial under the terms ofuse, the distribution, Creative Commons and reproduction Attribution in Non-Commercialany medium, provided License the(http://creativecommons.or original work is properly cited.g/licenses/by- nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 6298 | Christin et al. (Sage et al., 2011). These patterns indicate that some plant groups it is necessary to have a well-resolved, species-level phylogeny. have a higher propensity for C4 photosynthesis evolution, which Such a phylogeny was not available for the Neurachninae, as may reflect ecological, genomic, and/or anatomical factors that only some members of the group have been analysed with a small facilitate the acquisition of novel traits (Sage, 2001; Marshall number of molecular markers (Hudson et al., 1990; Christin et al., et al., 2007; McKown and Dengler, 2007; Christin et al., 2011; 2008; Grass Phylogeny Working Group II, 2012). Edwards and Ogburn, 2012). Leading environmental factors pro- The objective of the present study was a reconstruction of moting C4 evolution are low atmospheric CO2, heat, drought and the evolutionary history of the Neurachninae, with an emphasis salinity, often in combination (Sage et al., 2012). Anatomical on photosynthetic pathway evolution. Multiple accessions per factors include high vein density, which may be common in dry species were sampled, and phylogenetic analyses of plastid as environments and certain taxonomic groups such as the grasses well as nuclear markers, photosynthetic pathway identification,
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