Advertisement

Marine Biology

, 166:24 | Cite as

Within- and among-leaf variations in photo-physiological functions, gene expression and DNA methylation patterns in the large-sized seagrass Posidonia oceanica

  • Miriam RuoccoEmail author
  • Lázaro Marín-Guirao
  • Gabriele Procaccini
Original paper

Abstract

The knowledge of how molecular functions vary in relation to developmental and environmental cues within and among seagrass leaves is scarce in comparison with terrestrial angiosperms. This strongly limits the mechanistic understanding of photosynthetic development and light acclimation processes in seagrasses, besides having fundamental methodological implications when small leaf sections are utilized as a proxy for assessing the photosynthetic performance and molecular responses to environmental changes for the whole plant. Here, the expression gradients of genes associated with key plant metabolic processes (i.e. photosynthesis, energy dissipation mechanisms, stress response and programmed cell death) were determined, for the first time, in three segments (i.e. basal, medium and high) along the longitudinal axis of three ranked leaves (i.e. leaf 1, 2 and 3) in the large-sized seagrass Posidonia oceanica. The evaluation of major shifts in gene expression paralleled the analysis of photo-physiological properties and global DNA methylation level of the different leaf sections. Photo-physiological and molecular results converged in suggesting that the within-leaf (vertical) gradient was stronger than the leaf-rank (horizontal) gradient, likely reflecting the sharp irradiance attenuation occurring inside the complex canopy formed by this species. Specific correlations between target gene expression and photo-physiological measurements were found, providing a first description of molecular rearrangements underlying the differential photosynthetic performance and light acclimation capacity of seagrass leaves. DNA methylation varied with tissue age, being higher in the youngest and oldest leaf sections, while decreasing in intermediate tissues. We interpreted such changes as a consequence of the interplay between developmental and light cues.

Notes

Acknowledgements

MR was supported by a SZN Ph.D. fellowship via the Open University. We deeply thank Pasquale De Luca (SZN–Molecular Biology Service) for his invaluable technical support in RT-qPCR experiments. We are grateful to Özge Tutar and Roberto Gallia for their help with the mesocosm system maintenance and sample collection, the SZN–MARE service (MEDA unit) for the sampling of seagrass ramets, and Maurizio Ribera d’Alcalà for the kind provision of seawater spectra for setting LED lamp illumination.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

227_2019_3482_MOESM1_ESM.pdf (357 kb)
Supplementary material 1 (PDF 356 kb)

References

  1. Alcoverro T, Manzanera M, Romero J (1998) Seasonal and age-dependent variability of Posidonia oceanica (L.) Delile photosynthetic parameters. J Exp Mar Biol Ecol 230:1–13.  https://doi.org/10.1016/S0022-0981(98)00022-7 CrossRefGoogle Scholar
  2. Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Can Res 64:5245–5250.  https://doi.org/10.1158/0008-5472.can-04-0496 CrossRefGoogle Scholar
  3. Arnaud-Haond S, Duarte CM, Diaz-Almela E, Marbà N, Sintes T, Serrão EA (2012) Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica. PLoS One 7:e30454.  https://doi.org/10.1371/journal.pone.0030454 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta Bioenerg 1143:113–134.  https://doi.org/10.1016/0005-2728(93)90134-2 CrossRefGoogle Scholar
  5. Cahoon AB, Takacs EM, Sharpe RM, Stern DB (2008) Nuclear, chloroplast, and mitochondrial transcript abundance along a maize leaf developmental gradient. Plant Mol Biol 66:33–46.  https://doi.org/10.1007/s11103-007-9250-z CrossRefPubMedGoogle Scholar
  6. Candaele J, Demuynck K, Mosoti D, Beemster GTS, Inzé D, Nelissen H (2014) Differential methylation during maize leaf growth targets developmentally regulated genes. Plant Physiol 164:1350–1364.  https://doi.org/10.1104/pp.113.233312 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chang Y-M, Liu W-Y, Shih AC-C, Shen M-N, Lu C-H, Lu M-YJ, Yang H-W, Wang T-Y, Chen SC-C, Chen SM, Li W-H, Ku MSB (2012) Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiol 160:165–177.  https://doi.org/10.1104/pp.112.203810 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chinnusamy V, Zhu J-K (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139.  https://doi.org/10.1016/j.pbi.2008.12.006 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Clarke K, Gorley R (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  10. Costanza R, dArge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, Oneill R, Paruelo J (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260CrossRefGoogle Scholar
  11. Cullen-Unsworth LC, Nordlund LM, Paddock J, Baker S, McKenzieLJ Unsworth RK (2014) Seagrass meadows globally as a coupled social–ecological system: implications for human wellbeing. Mar Pollut Bull 83(2):387–397CrossRefGoogle Scholar
  12. D’Esposito D, Orrù L, Dattolo E, Bernardo L, Lamontanara A, Orsini L, Serra I, Mazzuca S, Procaccini G (2017) Transcriptome characterisation and simple sequence repeat marker discovery in the seagrass Posidonia oceanica. Sci Data 3:160115CrossRefGoogle Scholar
  13. Dalla Via J, Sturmbauer C, Schönweger G, Sötz E, Mathekowitsch S, Stifter M, Rieger R (1998) Light gradients and meadow structure in Posidonia oceanica: ecomorphological and functional correlates. Mar Ecol Prog Ser 163:267–278.  https://doi.org/10.3354/meps163267 CrossRefGoogle Scholar
  14. Dattolo E, Ruocco M, Brunet C, Lorenti M, Lauritano C, D’Esposito D, De Luca P, Sanges R, Mazzuca S, Procaccini G (2014) Response of the seagrass Posidonia oceanica to different light environments: insights from a combined molecular and photo-physiological study. Mar Environ Res 101:225–236.  https://doi.org/10.1016/j.marenvres.2014.07.010 CrossRefPubMedGoogle Scholar
  15. De Pinto M, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant Cell Environ 35:234–244CrossRefGoogle Scholar
  16. Durako MJ, Kunzelman JI (2002) Photosynthetic characteristics of Thalassia testudinum measured in situ by pulse-amplitude modulated (PAM) fluorometry: methodological and scale-based considerations. Aquat Bot 73:173–185.  https://doi.org/10.1016/S0304-3770(02)00020-7 CrossRefGoogle Scholar
  17. Enríquez S, Borowitzka MA (2010) The use of the fluorescence signal in studies of seagrasses and macroalgae. In: Suggett D, Prášil O, Borowitzka M (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 187–208CrossRefGoogle Scholar
  18. Enríquez S, Merino M, Iglesias-Prieto R (2002) Variations in the photosynthetic performance along the leaves of the tropical seagrass Thalassia testudinum. Mar Biol 140:891–900CrossRefGoogle Scholar
  19. Evert RF, Russin WA, Bosabalidis AM (1996) Anatomical and ultrastructural changes associated with sink-to-source transition in developing maize leaves. Int J Plant Sci 157:247–261CrossRefGoogle Scholar
  20. Finnegan PM, Soole KL, Umbach AL (2004) Alternative mitochondrial electron transport proteins in higher plants. In: Day DA, Millar AH, Whelan J (eds) Plant mitochondria: from genome to function. Springer, Dordrecht, pp 163–230CrossRefGoogle Scholar
  21. Golicz AA, Schliep M, Lee HT, Larkum AWD, Dolferus R, Batley J, Chan C-KK, Sablok G, Ralph PJ, Edwards D (2015) Genome-wide survey of the seagrass Zostera muelleri suggests modification of the ethylene signalling network. J Exp Bot 66:1489–1498.  https://doi.org/10.1093/jxb/eru510 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Greco M, Chiappetta A, Bruno L, Bitonti MB (2013) Effects of light deficiency on genome methylation in Posidonia oceanica. Mar Ecol Prog Ser 473:103–114CrossRefGoogle Scholar
  23. Guo Y, Gan S (2005) Leaf senescence: signals, execution, and regulation current topics in developmental biology. Academic Press, New York, pp 83–112Google Scholar
  24. Hammer Ø, Harper D, Ryan P (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontolia Electronica 4:9Google Scholar
  25. Jahnke M, Olsen JL, Procaccini G (2015) A meta-analysis reveals a positive correlation between genetic diversity metrics and environmental status in the long-lived seagrass Posidonia oceanica. Mol Ecol 24:2336–2348.  https://doi.org/10.1111/mec.13174 CrossRefPubMedGoogle Scholar
  26. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291.  https://doi.org/10.1093/bioinformatics/btm091 CrossRefPubMedGoogle Scholar
  27. Kuo J, Den Hartog C (2007) Seagrass morphology, anatomy, and ultrastructure. In: Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 51–87Google Scholar
  28. Larkum AWD, Orth RJ, Duarte CM (2006) Seagrasses: biology, ecology and conservation. Springer, Dordrecht  Google Scholar
  29. Lauritano C, Ruocco M, Dattolo E, Buia MC, Silva J, Santos R, Olivé I, Costa MM, Procaccini G (2015) Response of key stress-related genes of the seagrass Posidonia oceanica in the vicinity of submarine volcanic vents. Biogeosciences 12:4185–4194CrossRefGoogle Scholar
  30. Leech RM, Rumsby MG, Thomson WW (1973) Plastid differentiation, acyl lipid, and fatty acid changes in developing green maize leaves. Plant Physiol 52:240–245CrossRefGoogle Scholar
  31. Les DH, Cleland MA, Waycott M (1997) Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Syst Bot 22:443–463.  https://doi.org/10.2307/2419820 CrossRefGoogle Scholar
  32. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067CrossRefGoogle Scholar
  33. Li N, Chen Y-R, Ding Z, Li P, Wu Y, Zhang A, Yu S, Giovannoni JJ, Fei Z, Zhang W (2015) Nonuniform gene expression pattern detected along the longitudinal axis in the matured rice leaf. Sci Rep 5:8015CrossRefGoogle Scholar
  34. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Limited, LondonGoogle Scholar
  35. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136.  https://doi.org/10.1146/annurev.arplant.57.032905.105316 CrossRefPubMedGoogle Scholar
  36. Liu W-Y, Chang Y-M, Chen SC-C, Lu C-H, Wu Y-H, Lu M-YJ, Chen D-R, Shih AC-C, Sheue C-R, Huang H-C, Yu C-P, Lin H-H, Shiu S-H, Sun-Ben KuM, Li W-H (2013) Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination. Proc Natl Acad Sci 110:3979–3984.  https://doi.org/10.1073/pnas.1301009110 CrossRefPubMedGoogle Scholar
  37. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, Zhang C, Asakura Y, Bhuiyan NH, Sun Q, Turgeon R, van Wijk KJ (2010) Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell 22:3509–3542.  https://doi.org/10.1105/tpc.110.079764 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Major KM, Dunton KH (2002) Variations in light-harvesting characteristics of the seagrass, Thalassia testudinum: evidence for photoacclimation. J Exp Mar Biol Ecol 275:173–189.  https://doi.org/10.1016/S0022-0981(02)00212-5 CrossRefGoogle Scholar
  39. Marín-Guirao L, Sandoval-Gil JM, Ruíz JM, Sánchez-Lizaso JL (2011) Photosynthesis, growth and survival of the Mediterranean seagrass Posidonia oceanica in response to simulated salinity increases in a laboratory mesocosm system. Estuar Coast Shelf Sci 92:286–296.  https://doi.org/10.1016/j.ecss.2011.01.003 CrossRefGoogle Scholar
  40. Marín-Guirao Ruiz JM, Sandoval-GilJM Bernardeau-Esteller J, Stinco CM, Meléndez-Martínez A (2013) Xanthophyll cycle-related photoprotective mechanism in the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa under normal and stressful hypersaline conditions. Aquat Bot 109:14–24CrossRefGoogle Scholar
  41. Marín-Guirao L, Bernardeau-Esteller J, Ruiz JM, Sandoval JM (2015) Resistance of Posidonia oceanica seagrass meadows to the spread of the introduced green alga Caulerpa cylindracea: assessment of the role of light. Biol Invasions 17(7):1989–2009CrossRefGoogle Scholar
  42. Marín-Guirao L, Entrambasaguas L, Dattolo E, Ruiz JM, Procaccini G (2017) Molecular mechanisms behind the physiological resistance to intense transient warming in an iconic marine plant. Front Plant Sci.  https://doi.org/10.3389/fpls.2017.01142 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Marín-Guirao L, Bernardeau-Esteller J, García-Muñoz R, Ramos A, Ontoria Y, Romero J, Pérez M, Ruiz JM, Procaccini G (2018) Carbon economy of Mediterranean seagrasses in response to thermal stress. Mar Pollut Bull 135:617–629CrossRefGoogle Scholar
  44. Martineau B, Taylor WC (1985) Photosynthetic gene expression and cellular differentiation in developing maize leaves. Plant Physiol 78:399–404.  https://doi.org/10.1104/pp.78.2.399 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mateo M, Romero J (1997) Detritus dynamics in the seagrass Posidonia oceanica: elements for an ecosystem carbon and nutrient budget. Oceanogr Lit Rev 10:1106Google Scholar
  46. Mattiello L, Riaño-Pachón DM, Martins MCM, da Cruz LP, Bassi D, Marchiori PER, Ribeiro RV, Labate MTV, Labate CA, Menossi M (2015) Physiological and transcriptional analyses of developmental stages along sugarcane leaf. BMC Plant Biol 15:300.  https://doi.org/10.1186/s12870-015-0694-z CrossRefPubMedPubMedCentralGoogle Scholar
  47. Mazzella L, Alberte RS (1986) Light adaptation and the role of autotrophic epiphytes in primary production of the temperate seagrass, Zostera marina L. J Exp Mar Biol Ecol 100:165–180CrossRefGoogle Scholar
  48. Mazzella L, Mauzerall D, Alberte R (1980) Photosynthetic light adaptation features of Zostera marina L (eelgrass). In: Biological bulletin. Marine biological laboratory, MA, pp 500–500Google Scholar
  49. Mullet JE (1988) Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39:475–502.  https://doi.org/10.1146/annurev.pp.39.060188.002355 CrossRefGoogle Scholar
  50. Mulo P, Sakurai I, Aro E-M (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochimica et Biophysica Acta Bioenerg 1817:247–257.  https://doi.org/10.1016/j.bbabio.2011.04.011 CrossRefGoogle Scholar
  51. Munekage Y, Hashimoto M, Miyake C, Tomizawa K-I, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582CrossRefGoogle Scholar
  52. Niederhuth CE, Schmitz RJ (2017) Putting DNA methylation in context: from genomes to gene expression in plants. Biochimica et Biophysica Acta Gene Regul Mech 1860:149–156.  https://doi.org/10.1016/j.bbagrm.2016.08.009 CrossRefGoogle Scholar
  53. Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382.  https://doi.org/10.1093/jxb/eri056 CrossRefPubMedGoogle Scholar
  54. Olivé I, Vergara J, Pérez-Lloréns J (2013) Photosynthetic and morphological photoacclimation of the seagrass Cymodocea nodosa to season, depth and leaf position. Mar Biol 160:285–297CrossRefGoogle Scholar
  55. Olsen JL, Rouzé P, Verhelst B, Lin Y-C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Töpel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Boström C, Chovatia M, Grimwood J, Jenkins JW, Jueterbock A, Mraz A, Stam WT, Tice H, Bornberg-Bauer E, Green PJ, Pearson GA, Procaccini G, Duarte CM, Schmutz J, Reusch TBH, Van de Peer Y (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530:331–335.  https://doi.org/10.1038/nature16548 CrossRefPubMedGoogle Scholar
  56. Pfaffl M, Tichopad A, Prgomet C, Neuvians T (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515.  https://doi.org/10.1023/B:BILE.0000019559.84305.47 CrossRefPubMedGoogle Scholar
  57. Pick TR, Bräutigam A, Schlüter U, Denton AK, Colmsee C, Scholz U, Fahnenstich H, Pieruschka R, Rascher U, Sonnewald U, Weber APM (2011) Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell 23:4208–4220.  https://doi.org/10.1105/tpc.111.090324 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Procaccini G, Ruocco M, Marín-Guirao L, Dattolo E, Brunet C, D’Esposito D, Lauritano C, Mazzuca S, Serra IA, Bernardo L, Piro A, Beer S, Björk M, Gullström M, Buapet P, Rasmusson LM, Felisberto P, Gobert S, Runcie JW, Silva J, Olivé I, Costa MM, Barrote I, Santos R (2017) Depth-specific fluctuations of gene expression and protein abundance modulate the photophysiology in the seagrass Posidonia oceanica. Sci Rep 7:42890.  https://doi.org/10.1038/srep42890 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ralph PJ, Gademann R (1999) Photosynthesis of the seagrass Posidonia australis Hook. f. and associated epiphytes, measured by in situ fluorescence analysis. In: Seagrass flora and fauna of Rottnest Island, Western Australia, pp 63–71Google Scholar
  60. Ralph P, Polk S, Moore K, Orth R, Smith W (2002) Operation of the xanthophyll cycle in the seagrass Zostera marina in response to variable irradiance. J Exp Mar Biol Ecol 271:189–207CrossRefGoogle Scholar
  61. Ralph PJ, Durako MJ, Enríquez S, Collier CJ, Doblin MA (2007) Impact of light limitation on seagrasses. J Exp Mar Biol Ecol 350:176–193.  https://doi.org/10.1016/j.jembe.2007.06.017 CrossRefGoogle Scholar
  62. Richards EJ (1997) DNA methylation and plant development. Trends Genet 13:319–323.  https://doi.org/10.1016/S0168-9525(97)01199-2 CrossRefPubMedGoogle Scholar
  63. Robson CA, Vanlerberghe GC (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol 129:1908CrossRefGoogle Scholar
  64. Ruocco M, Marín-Guirao L, Ravaglioli C, Bulleri F, Procaccini G (2018) Molecular level responses to chronic versus pulse nutrient loading in the seagrass Posidonia oceanica undergoing herbivore pressure. Oecologia 188:23CrossRefGoogle Scholar
  65. Sandoval-Gil JM, Ruiz JM, Marin-Guirao L, Bernardeau-Esteller J, Sanchez-Lizaso JL (2014) Ecophysiological plasticity of shallow and deep populations of the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa in response to hypersaline stress. Mar Environ Res 95:39–61.  https://doi.org/10.1016/j.marenvres.2013.12.011 CrossRefPubMedGoogle Scholar
  66. Schubert N, Colombo-Pallota MF, Enríquez S (2015) Leaf and canopy scale characterization of the photoprotective response to high-light stress of the seagrass Thalassia testudinum. Limnol Oceanogr 60:286–302.  https://doi.org/10.1002/lno.10024 CrossRefGoogle Scholar
  67. Serra IA, Lauritano C, Dattolo E, Puoti A, Nicastro S, Innocenti AM, Procaccini G (2012) Reference genes assessment for the seagrass Posidonia oceanica in different salinity, pH and light conditions. Mar Biol 159:1269–1282CrossRefGoogle Scholar
  68. Sharman B (1942) Developmental anatomy of the shoot of Zea mays L. Ann Bot 6:245–282CrossRefGoogle Scholar
  69. Svensson ÅS, Rasmusson AG (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J 28:73–82CrossRefGoogle Scholar
  70. Tolley BJ, Woodfield H, Wanchana S, Bruskiewich R, Hibberd JM (2012) Light-regulated and cell-specific methylation of the maize PEPC promoter. J Exp Bot 63:1381–1390.  https://doi.org/10.1093/jxb/err367 CrossRefPubMedGoogle Scholar
  71. Traboni C, Mammola SD, Ruocco M, Ontoria Y, Ruiz JM, Procaccini G, Marín-Guirao L (2018) Investigating cellular stress response to heat stress in the seagrass Posidonia oceanica in a global change scenario. Mar Environ Res.  https://doi.org/10.1016/j.marenvres.2018.07.007 CrossRefPubMedGoogle Scholar
  72. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40:e115–e115.  https://doi.org/10.1093/nar/gks596 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Valière N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2(3):377–379Google Scholar
  74. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1–12.  https://doi.org/10.1186/gb-2002-3-7-research0034 CrossRefGoogle Scholar
  75. Vanlerberghe GC, Robson CA, Yip JYH (2002) Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol 129:1829CrossRefGoogle Scholar
  76. Vishwakarma A, Bashyam L, Senthilkumaran B, Scheibe R, Padmasree K (2014) Physiological role of AOX1a in photosynthesis and maintenance of cellular redox homeostasis under high light in Arabidopsis thaliana. Plant Physiol Biochem 81:44–53CrossRefGoogle Scholar
  77. Vishwakarma A, Tetali SD, Selinski J, Scheibe R, Padmasree K (2015) Importance of the alternative oxidase (AOX) pathway in regulating cellular redox and ROS homeostasis to optimize photosynthesis during restriction of the cytochrome oxidase pathway in Arabidopsis thaliana. Ann Bot 116:555–569CrossRefGoogle Scholar
  78. Wang L, Czedik-Eysenberg A, Mertz RA, Si Y, Tohge T, Nunes-Nesi A, Arrivault S, Dedow LK, Bryant DW, Zhou W, Xu J, Weissmann S, Studer A, Li P, Zhang C, LaRue T, Shao Y, Ding Z, Sun Q, Patel RV, Turgeon R, Zhu X, Provart NJ, Mockler TC, Fernie AR, Stitt M, Liu P, Brutnell TP (2014) Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice. Nat Biotechnol 32:1158.  https://doi.org/10.1038/nbt.3019 CrossRefPubMedGoogle Scholar
  79. Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884–894CrossRefGoogle Scholar
  80. Waycott M, Procaccini G, Les DH, Reusch TBH (2007) Seagrass evolution, ecology and conservation: a genetic perspective. In: Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 25–50Google Scholar
  81. Wissler L, Codoner FM, Gu J, Reusch TB, Olsen JL, Procaccini G, Bornberg-Bauer E (2011) Back to the sea twice: identifying candidate plant genes for molecular evolution to marine life. BMC Evol Biol 11:8.  https://doi.org/10.1186/1471-2148-11-8 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Yoshida K, Noguchi K (2009) Differential gene expression profiles of the mitochondrial respiratory components in illuminated Arabidopsis leaves. Plant Cell Physiol 50:1449–1462CrossRefGoogle Scholar
  83. Yu CP, Chen SCC, Chang YM, Liu WY, Lin HH, Lin JJ, Chen HJ, Lu YJ, Wu YH, Lu MYJ, Lu C-H, Shih ACC, Ku MSB, Shiu SH, Wu SH, Li WH (2015) Transcriptome dynamics of developing maize leaves and genome wide prediction of cis elements and their cognate transcription factors. Proc Natl Acad Sci 112:E2477–E2486.  https://doi.org/10.1073/pnas.1500605112 CrossRefPubMedGoogle Scholar
  84. Zhang M, Kimatu JN, Xu K, Liu B (2010) DNA cytosine methylation in plant development. J Genet Genom 37:1–12.  https://doi.org/10.1016/S1673-8527(09)60020-5 CrossRefGoogle Scholar
  85. Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2011) Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Plant 143:396–407CrossRefGoogle Scholar
  86. Zhang L-T, Zhang Z-S, Gao H-Y, Meng X-L, Yang C, Liu J-G, Meng Q-W (2012) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:40CrossRefGoogle Scholar
  87. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2006) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61.  https://doi.org/10.1038/ng1929 CrossRefPubMedGoogle Scholar
  88. Zimmerman RC (2007) Light and photosynthesis in seagrass meadows seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 303–321Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Stazione Zoologica Anton DohrnNaplesItaly

Personalised recommendations