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A proteomic approach to seasonal adjustment in the enzyme complement of Korean fir (Abies koreana Wilson) needles

  • Soonja Oh
  • William W. AdamsIII
  • Barbara Demmig-Adams
  • Seok Chan Koh
Research Report
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Abstract

Korean fir is an endemic ornamental tree species facing population decline in Korea. To further understand the acclimatory adjustments it undergoes in response to seasonal extremes, we characterized some of the needle proteins that are upregulated during winter. Two-dimensional gel electrophoresis (2-DE), followed by MALDI TOF/TOF MS/MS and Mascot analyses, was used to visualize changes in protein profiles during acclimation to winter stress. From the 2-DE protein profiles of Korean fir needles, 226 protein spots were detected, many of which accumulated at higher levels during the winter. Among 17 proteins identified, 12 matched proteins associated with photosynthesis and with biotic and abiotic stresses, and eight were significantly upregulated under winter stress. Upregulated proteins included photosynthetic enzymes sedoheptulose-1,7-bisphosphatase and fructose bisphosphate aldolase of the Calvin–Benson cycle, four proteins related to oxidative stress tolerance, two proteins implicated in biotic defense, one heat-shock protein, and five unknown proteins. However, two other oxidative-stress-related proteins were present at high levels throughout the year, and a chitinase and the small subunit of ribulose-1,5-bisphosphate carboxylase showed no seasonal adjustments. Thus, Korean fir needles exhibited winter upregulation of some photosynthetic enzymes, coupled with increased photo protective thermal energy dissipation, and proteins related to abiotic and biotic stress resistance. Winter stress, which can include both low temperature and reduced water availability, in the subalpine region of Mount Halla led to an altered physiological equilibrium with increases in key Calvin–Benson cycle enzymes and increased enzymatic and non-enzymatic protection against oxidative stress.

Keywords

2-DE protein profiles Antioxidant enzymes Photosynthetic enzymes Photoprotective energy dissipation Winter stress 

Notes

Acknowledgements

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2011-0361) and the University of Colorado.

References

  1. Adams WW III, Demmig-Adams B (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiol Plant 92:451–458CrossRefGoogle Scholar
  2. Adams WW III, Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Environ 18:117–127CrossRefGoogle Scholar
  3. Adams WW III, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2006) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams WW III, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. Advances in photosynthesis and respiration, vol 21. Springer, Dordrecht, pp 49–64Google Scholar
  4. Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH (1995a) ‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–276Google Scholar
  5. Adams WW III, Hoehn A, Demmig-Adams B (1995b) Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach. Aust J Plant Physiol 22:75–85Google Scholar
  6. Adams WWIII, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biol 4:545–557CrossRefGoogle Scholar
  7. Adams WW III, Cohu CM, Muller O, Demmig-Adams B (2013) Foliar phloem infrastructure in support of photosynthesis. Front Plant Sci 4:194PubMedPubMedCentralGoogle Scholar
  8. Adams WW III, Stewart JJ, Cohu CM, Muller O, Demmig-Adams B (2016) Habitat temperature and precipitation of Arabidopsis thaliana ecotypes determine the response of foliar vasculature, photosynthesis, and transpiration to growth temperature. Front Plant Sci 7:1026CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bartoli CG, Casalongué CA, Simontacchi M, Marquez-Garcia B, Foyer CH (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 34:73–88CrossRefGoogle Scholar
  10. Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543CrossRefGoogle Scholar
  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  12. Cho HK, Miyamoto T, Takahashi K, Hong SG, Kim JJ (2007) Damage to Abies koreana seeds by soil-borne fungi on Mount Halla, Korea. Can J For Res 37:371–382CrossRefGoogle Scholar
  13. Cohu CM, Muller O, Stewart JJ, Demmig-Adams B, Adams WW III (2013) Association between minor loading vein architecture and light- and CO2-saturated photosynthetic oxygen evolution among Arabidopsis thaliana ecotypes from different latitudes. Front Plant Sci 4:264PubMedPubMedCentralGoogle Scholar
  14. Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172CrossRefPubMedGoogle Scholar
  15. Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal dissipation. New Phytol 172:11–21CrossRefPubMedGoogle Scholar
  16. Demmig-Adams B, Cohu CM, Muller O, Adams WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88CrossRefPubMedGoogle Scholar
  17. Demmig-Adams B, Stewart JJ, Adams WW III (2014) Multiple feedbacks between chloroplast and whole plant in the context of plant adaptation and acclimation to the environment. Phil Trans R Soc B 369:20130244CrossRefPubMedGoogle Scholar
  18. Duffy CDP, Chmeliov J, Macernis M, Sulskus J, Valkunas L, Ruban AV (2013) Modeling of fluorescence quenching by lutein in the plant light-harvesting complete LHCII. J Phys Chem B 117:10974–10986CrossRefPubMedGoogle Scholar
  19. Ekramoddoullah AKM, Yu X, Sturrock R, Zamani A, Taylor D (2000) Detection and seasonal expression pattern of a pathogenesis-related protein (PR-10) in Douglas fir (Pseudotsuga menziesii) tissues. Physiol Plant 110:240–247CrossRefGoogle Scholar
  20. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100CrossRefPubMedGoogle Scholar
  21. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883CrossRefPubMedPubMedCentralGoogle Scholar
  22. Galindo-González LM, El Kayal W, Morris JS, Cooke JEK (2015) Diverse chitinases are invoked during the activity-dormancy transition in spruce. Tree Genet Genomes 11:41CrossRefGoogle Scholar
  23. Harris GC, Antoine V, Chan M, Nevidomskyte D, Königer M (2006) Seasonal changes in photosynthesis, protein composition and mineral content in Rhododendron leaves. Plant Sci 170:314–325CrossRefGoogle Scholar
  24. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052CrossRefPubMedGoogle Scholar
  25. Horton P (2012) Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences. Phil Trans R Soc B 367:3455–3465CrossRefPubMedGoogle Scholar
  26. Hoshino T, Xiao N (2009) Cold adaptation in the phytopathogenic fungi causing snow molds. Mycoscience 50:26–38CrossRefGoogle Scholar
  27. Ilioaia C, Johnson MP, Liao PN, Pascal AA, van Grondelle R, Walla PJ, Ruban AV, Robert B (2011) Photoprotection in plants involves a change in lutein 1 binding domain in the major light-harvesting complex of photosystem II. J Biol Chem 286:27247–27254CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ilioaia C, Duffy CDP, Johnson MP, Ruban AV (2013) Changes in the energy transfer pathways within photosystem II antenna induced by xanthophyll cycle activity. J Phys Chem B 117:5841–5947CrossRefPubMedGoogle Scholar
  29. IUCN (2013) IUCN Red List of Threatened Species. Version 2013. 2. http://www.iucnredlist.org. Accessed 7 September 2010
  30. Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotech J 15:405–414CrossRefGoogle Scholar
  31. Kang YJ, Kim SC, Kim WW, Kim CS, Park YB (1990) Variation of cone and needle characteristics of Abies koreana along the elevation gradients in Mt. Halla. Res Rep Inst For Gen Korea 26:119–123Google Scholar
  32. Kjellsen TD, Shiryaeva L, Schöder WP, Strimbeck GR (2010) Proteomics of extreme freezing tolerance in Siberian spruce (Picea obovata). J Proteomics 73:965–975CrossRefPubMedGoogle Scholar
  33. Kocsy G, Tari I, Vanková R, Zechmann B, Gulyás Z, Poór P, Galiba G (2013) Redox control of plant growth and development. Plant Sci 211:77–91CrossRefPubMedGoogle Scholar
  34. Koh SC, Demmig-Adams B, Adams WW III (2009) Novel patterns of seasonal photosynthetic acclimation, including interspecific differences, in conifers over an altitudinal gradient. Arct Antarct Alp Res 41:317–322CrossRefGoogle Scholar
  35. Kopczewski T, Kuzniak E (2013) Redox signals as a language of interorganellar communication in plant cells. Cent Eur J Biol 8:1153–1163Google Scholar
  36. Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress: contribution of proteomics studies to understanding plant stress response. J Proteomics 74:1301–1322CrossRefPubMedGoogle Scholar
  37. Kuwabara C, Imai R (2009) Molecular basis of disease resistance acquired through cold acclimation in overwintering plants. J Plant Biol 52:19–26CrossRefGoogle Scholar
  38. Lee TB (1986) Endemic plants and their distribution in Korea. J Natl Acad Sci Korea 21:169–218Google Scholar
  39. Lee WT (1996) Lineamenta Florae Koreae. Academy Press, Seoul, p 113Google Scholar
  40. Lee DH, Lee IC, Kim KJ, Kim DS, Na HJ, Lee I-J, Kang S-M, Jeon H-W, Le PY, Ko J-H (2014) Expression of gibberellin 2-oxidase 4 from Arabidopsis under the control of a senescence-associated promoter results in a dominant semi-dwarf plant with normal flowering. J Plant Biol 57:106–116CrossRefGoogle Scholar
  41. Liu J-J, Ekramoddoullah AKM (2004) Characterization, expression and evolution of two novel subfamilies of Pinus monticola cDNAs encoding pathogenesis-related (PR)-10 proteins. Tree Physiol 24:1377–1385CrossRefPubMedGoogle Scholar
  42. Liu J-J, Ekramoddoullah AKM, Yu X (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant 119:544–553CrossRefGoogle Scholar
  43. Logan BA, Kornyeyev D, Hardison J, Holaday AS (2006) The role of antioxidant enzymes in photoprotection. Photosynth Res 88:119–132CrossRefPubMedGoogle Scholar
  44. Matsumoto N (1994) Ecological adaptations of low temperature plant pathogenic fungi to diverse winter climates. Can J Plant Pathol 16:237–240CrossRefGoogle Scholar
  45. Oakley BR, Kirsch DR, Morris NR (1980) A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal Biochem 105:361–363CrossRefPubMedGoogle Scholar
  46. Oh SJ, Koh JG, Kim ES, Oh MY, Koh SC (2001) Diurnal and seasonal variation of chlorophyll fluorescence from Korean fir plants on Mt. Halla. Kor J Environ Biol 19:43–48Google Scholar
  47. Oh SJ, Adams WW III, Demmig-Adams B, Koh SC (2013) Seasonal photoprotective responses in needles of Korean fir (Abies koreana) over an altitudinal gradient on Mount Halla, Jeju Island, Korea. Arct Antarct Alp Res 45:238–248CrossRefGoogle Scholar
  48. Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181CrossRefPubMedGoogle Scholar
  49. Saravana RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4:2522–2532CrossRefGoogle Scholar
  50. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68:850–858CrossRefPubMedGoogle Scholar
  51. Skyba M, Petijova L, Kosuth J, Koleva DP, Ganeva TG, Kapchina-Toteva VM, Cellarova E (2012) Oxidative stress and antioxidant response in Hypericum perforatum L. plants subjected to low temperature treatment. J Plant Physiol 169:955–964CrossRefPubMedGoogle Scholar
  52. Stone JK, Hood A, Watt MS, Kerrigan JL (2007) Distribution of Swiss needle cast in New Zealand in relation to winter temperature. Aust Plant Pathol 36:445–454CrossRefGoogle Scholar
  53. Sundar D, Chaitanya KV, Jutur PP, Reddy AR (2004) Low temperature induced changes in antioxidative metabolism in rubber-producing shrub, guayule (Parthenium argentatum Gray). Plant Growth Regul 44:175–181CrossRefGoogle Scholar
  54. Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis HSP70 gene family. Plant Physiol 126:789–800CrossRefPubMedPubMedCentralGoogle Scholar
  55. Thayer S, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23:331–343CrossRefPubMedGoogle Scholar
  56. Ukaji N, Kuwabara C, Takezawa D, Arakawa K, Fujikawa S (2004) Accumulation of pathogenesis-related (PR) 10/Bet v 1 protein homologues in mulberry (Morus bombycis Koidz.) tree during winter. Plant, Cell Environ 27:1112–1121CrossRefGoogle Scholar
  57. Verhoeven AS, Adams WW III, Demmig-Adams B (1996) Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. Physiol Plant 96:567–576CrossRefGoogle Scholar
  58. Wäli PR, Helander M, Nissinen O, Saikkonen K (2006) Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Can J Bot 84:1043–1051CrossRefGoogle Scholar
  59. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Roles of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252CrossRefPubMedPubMedCentralGoogle Scholar
  60. Woo SY, Lim JW, Lee DK (2008) Effects of temperature on photosynthetic rates in Korean fir (Abies koreana) between healthy and dieback population. J Integr Plant Biol 50:129–152CrossRefGoogle Scholar
  61. Xi J, Wang X, Li S, Zhou X, Yue L, Fan J, Hao D (2006) Polyethylene glycol fractionation improved detection of low-abundant proteins by two-dimensional electrophoresis analysis of plant proteome. Phytochemistry 67:2341–2348CrossRefPubMedGoogle Scholar
  62. Xing WB, Rajashekar CB (2001) Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Environ Exp Bot 46:21–28CrossRefPubMedGoogle Scholar
  63. Yamazaki JY, Tsuchiya S, Nagano S, Maruta E (2007) Photoprotective mechanisms against winter stress in the needles of Abies mariesii grown at the tree line on Mt. Norikura in Central Japan. Photosynthetica 45:547–554CrossRefGoogle Scholar
  64. Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117CrossRefPubMedGoogle Scholar
  65. Yan JQ, Wang J, Zhang H (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J 29:193–202CrossRefPubMedGoogle Scholar
  66. Zarter CR, Adams WW III, Ebbert V, Cuthbertson D, Adamska I, Demmig-Adams B (2006a) Winter downregulation of intrinsic photosynthetic capacity coupled with upregulation of Elip-like proteins and persistent energy dissipation in a subalpine forest. New Phytol 172:272–282CrossRefPubMedGoogle Scholar
  67. Zarter CR, Demmig-Adams B, Ebbert V, Adamska I, Adams WW III (2006b) Photosynthetic capacity and light harvesting efficiency during the winter-to-spring transition in subalpine conifers. New Phytol 172:283–292CrossRefPubMedGoogle Scholar
  68. Zarter CR, Adams WW III, Ebbert V, Adamska I, Jansson S, Demmig-Adams B (2006c) Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment. Plant, Cell Environ 29:869–878CrossRefGoogle Scholar
  69. Zeng Y, Yu J, Cang J, Liu LJ, Mu YC, Wang JH, Zhang D (2011) Detection of sugar accumulation and expression levels of correlative key enzymes in winter wheat (Triticum aestivum) at low temperatures. Biosci Biotech Bioch 75:681–687CrossRefGoogle Scholar
  70. Zhang Q, Zhang JZ, Chow WS, Sun LL, Chen JW, Chen YJ (2011) The influence of low temperature on photosynthesis and antioxidant enzymes in sensitive banana and tolerant plantain (Musa sp.) cultivars. Photosynthetica 49:201–208CrossRefGoogle Scholar
  71. Zhang W, Zhao X, Shi M, Yang A, Hua B, Liu Y (2016) Altered protein expression in peach (Prunus persica) following fruit bagging. Korean J Hortic Sci Technol 34:32–45Google Scholar

Copyright information

© Korean Society for Horticultural Science 2018

Authors and Affiliations

  1. 1.Agricultural Research Center for Climate Change, RDAJejuKorea
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  3. 3.Department of Biology and Research Institute for Basic SciencesJeju National UniversityJejuKorea

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