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Anatomical Basis of Variation in Mesophyll Resistance in Eastern

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Anatomical Basis of Variation in Mesophyll Resistance in Eastern Journal of Experimental Botany , Vol. 63, 63, No. No. 14, 2, pp. pp. 695–709, 5105–5119, 2012 2012 doi:10.1093/jxb/err313doi:10.1093/jxb/ers171 Advance Advance Access Access publication publication 9 4August, November, 2012 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) RESEARCH PAPER InAnatomicalPosidonia basis oceanica of variationcadmium in mesophyll induces changes resistance in DNA methylationin eastern Australian and chromatin sclerophylls: patterning news of a long and winding path Maria Greco, Adriana Chiappetta, Leonardo Bruno and Maria Beatrice Bitonti* DepartmentTiina Tosens of Ecology,1,2,*, Ülo UniversityNiinemets of Calabria,2, Mark LaboratoryWestoby1 of and Plant Ian Cyto-physiology, J. Wright1 Ponte Pietro Bucci, I-87036 Arcavacata di Rende, Cosenza, Italy 1 Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia * To whom correspondence should be addressed. E-mail: [email protected] 2 Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 64, Tartu 51014, Estonia Downloaded from Received*To whom 29 correspondence May 2011; Revised should 8 July be 2011;addressed. Accepted E-mail: 18 August [email protected] 2011 Received 13 March 2012; Revised 27 April 2012; Accepted 4 May 2012 Abstract InAbstract mammals, cadmium is widely considered as a non-genotoxic carcinogen acting through a methylation-dependent http://jxb.oxfordjournals.org/ epigenetic mechanism. Here, the effects of Cd treatment on the DNA methylation patten are examined together with itsIn sclerophylls, effect on chromatin photosynthesis reconfiguration is particularly in Posidonia strongly limited oceanica by. mesophyll DNA methylation diffusion level resistance and pattern from substomatal were analysed cavi in- activelyties to chloroplasts growing organs, (rm), but under theshort- controls (6 h)on and diffusion long- (2limits d or by 4 d) integral term and leaf low variables (10 mM) such and as high leaf (50 thickness,mM) doses density, of Cd, throughand dry mass a Methylation-Sensitive per unit area and by the Amplification individual steps Polymorphism along the diffusion technique pathway and are an imperfectly immunocytological understood. approach, To gain respectively.insight into the The determinants expression of of rm one in leaves member with of varying the CHROMOMETHYLASE structure, the full CO2 (physicalCMT) family, diffusion a DNA pathway methyltransferase, was analysed wasin 32 alsoAustralian assessed species by sampled qRT-PCR. from Nuclear sites contrasting chromatin in ultrastructure soil nutrients was and investigatedrainfall, and having by transmission leaf structures electron from microscopy.mesophytic to Cd strongly treatment sclerophyllous. induced a DNArm was hypermethylation, estimated based ason wellcombined as an measurements up-regulation ofof CMTgas exchange, indicating and that chlode- at Macquarie University on January 31, 2013 novorophyllmethylation fluorescence. did In indeed addition, occur. rm was Moreover, modelled a on high the dose basis of of Cd detailed led to anatomical a progressive measurements heterochromatinization to separate the of interphaseimportance nucleiof different and apoptotic serial resistances figures were affecting also observed CO2 diffusion after into long-term chloroplasts. treatment. The Thestrongest data demonstrate sources of variation that Cd perturbsin rm were the Sc/S DNA, the methylationexposed surface status area through of chloroplasts the involvement per unit ofleaf a area, specific andmethyltransferase. mesophyll cell wall Suchthickness, changes tcw. The are linkedstrong correlation to nuclear of chromatin rm with tcw reconfiguration could not be explained likely to by establish cell wall athickness new balance alone, of and expressed/repressed most likely arose from chromatin. a further Overall,effect of thecell data wall showporosity. an epigeneticThe CO2 drawdown basis to thefrom mechanism intercellular underlying spaces to Cd chloroplasts toxicity in plants.was positively correlated with tcw, suggesting enhanced diffusional limitations in leaves with thicker cell walls. Leaf thickness and density were poorly Keycorrelated words: with5-Methylcytosine-antibody, Sc/S, indicating that widely cadmium-stress varying combinations condition, chromatin of leaf anatomical reconfiguration, traitsCHROMOMETHYLASE occur at given values, of leaf DNA-methylation,integrated traits, Methylation-and suggesting Sensitive that Amplificationdetailed anatomical Polymorphism studies (MSAP), are neededPosidonia to predict oceanica rm (L.)for Delile.any given species. Key words: Anatomical model, cell wall thickness, diffusion limitations of photosynthesis, interspecific variability, leaf economics spectrum, mesophyll diffusion. Introduction In the Mediterranean coastal ecosystem, the endemic Although not essential for plant growth, in terrestrial seagrassIntroductionPosidonia oceanica (L.) Delile plays a relevant role plants, Cd is readily absorbed by roots and translocated into by ensuring primary production, water oxygenation and aerial organs while, in acquatic plants, it is directly taken up providesLeaf photosynthesis niches for is somedetermined animals, by biochemical besides counteracting limitations byenzyme leaves. Rubisco. In plants, First, Cd CO absorption2 must diffuse induces through complex the intercel changes- coastal(photosynthetic erosion throughcapacity) its and widespread diffusion meadows limitations, (Ott, includ 1980;- atlular the airspaces genetic, to biochemical a mesophyll andcell surfaces physiological adjacent levels to the which air- Piazziing stomatalet al. ,resistance 1999; Alcoverro and CO2 diffusionet al., 2001). resistance There from is sub- also ultimatelyspace to enable account free foraccess its toxicityfor the CO (Valle2. Gas and diffusion Ulmer, in 1972; the considerablestomatal cavities evidence to the carboxylating that P. oceanica enzyme,plants Rubisco, are able in the to Sanitliquid phasedi Toppi is slow, and therefore Gabrielli, CO 1999; is most Benavides likely etto al.enter, 2005; the z 2 absorbchloroplasts and (so-called accumulate ‘mesophyll metals diffusion from sediments resistance’) (Sanchiz (Flexas Webercell whereet the al. ,chloroplast 2006; Liu directlyet al. ,abuts 2008). the Thecell wall most (Terashima obvious et al al..,, 2008, 1990; 2012; Pergent-Martini, Terashima et 1998; al., 2006, Maserti 2011).et al.The, 2005)concept thus of symptomet al., 2006, of Cd2011). toxicity This isprocess a reduction could inbe plant greatly growth enhanced due toif influencingmesophyll resistance metal bioavailability (rm, see Table 1 in for the symbol marine definitions) ecosystem. can anthe cell inhibition walls were of photosynthesis,fully lined with chloroplasts, respiration, a andcondition nitrogen that Forbe described this reason, as follows. this seagrassAfter entering is widely the leaf considered through the to sto be- metabolism,in practice is rare as well(Terashima as a reduction et al., 2006). in CO water2 dissolves and mineral in the amata, metal CO bioindicator2 faces a relatively species long (Maserti and tortuouset al. pathway, 1988; Pergentthrough uptakewater-filled (Ouzonidou pores ofet the al. ,cell 1997; wall Perfus-Barbeoch (Evans et al., 2009)et al. and, 2000; dif- etgas al.and, 1995;liquid phases Lafabrie beforeet it al. finally, 2007). reaches Cd isthe one carboxylating of most Shuklafuses acrosset al. the, 2003; cell Sobkowiakwall. Diffusion and across Deckert, cell 2003). walls is slow if 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 © The Author [2012]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: ª[email protected] The Author(s). This is anan OpenOpen AccessAccess articlearticle distributed distributed under under the the terms terms of of the the Creative Creative Commons Commons Attribution Attribution Non-Commercial Non-Commercial License License (http://creativecommons.or (http://creativecommons.org/licenses/g/licenses/by- nc/3.0),by-nc/2.0/uk/) which permitswhich permits unrestricted unrestricted non-commercial non-commercial use, distribution, use, distribution, and reproduction and reproduction in any in medium, any medium, provided provided the original the original work iswork properly is properly cited. cited. 5106 | Tosens et al. Table 1. Symbols and units used Variable Definition Unit A Net assimilation rate µmol m–2 s–1 –1 Cc CO2 concentration in chloroplasts µmol mol –1 Ci CO2 concentration in intercellular airspace µmol mol –1 Ci–Cc CO2 drawdown from intercellular airspace to chloroplasts µmol mol 2 –1 Da Diffusion coefficient for CO2 in the gas phase m s –3 dleaf Leaf density g cm 2 –1 Dw Aqueous phase diffusion coefficient for CO2 m s fias Fraction of mesophyll occupied by intercellular airspace Dimensionless fpal Fraction of mesophyll cell volume comprised of palisade tissue Dimensionless H/(RTk) Henry´s law constant Dimensionless ∆Lias Effective diffusion path length in the gas-phase m Lmes Total length of chloroplasts facing the intercellular airspace m Lmes Total length of mesophyll cells facing the intercellular
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