Journal of Ecology and Environment

The Ecological Society of Korea (한국생태학회)
권호 표지
DOI QR코드

DOI QR Code

Ecophysiological characteristics of Rosa rugosa under different environmental factors

  • Young-Been Kim (Department of Integrative Natural Sciences for the East Sea Rim, Kyungpook National University) ;
  • Sung-Hwan Yim (Department of Biology, Kyungpook National University) ;
  • Young-Seok Sim (Department of Biology, Kyungpook National University) ;
  • Yeon-Sik Choo (Department of Integrative Natural Sciences for the East Sea Rim, Kyungpook National University)
  • Received : 2023.07.03
  • Accepted : 2023.07.29
  • Published : 2023.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Ecophysiological characteristics of Rosa rugosa were analyzed under different environmental factors from May to October 2022. Photosynthesis, chlorophyll fluorescence, chlorophyll content, leaf water content (LWC), osmolality, carbohydrate content, and total ion content were measured to compare the physiological characteristics of R. rugosa at two study sites (i.e., in large pots and in the Goraebul coastal sand dune area). Results: When R. rugosa was exposed to high temperatures, photosynthetic parameters including net photosynthetic rate (PN) and stomatal conductance (gs) in both experiment areas declined. In addition, severe photoinhibition occurs when R. rugosa is continuously exposed to high photosynthetically active radiation (PAR), and because of this, relatively low Y(II) (i.e., the quantum yield of photochemical energy conversion in photosystem II [PSII]) and high Y(NO) (i.e., the quantum yield of non-regulated, non-photochemical energy loss in PSII) in the R. rugosa of the pot were observed. As the high Y(NPQ) (i.e., the quantum yield of regulated non-photochemical energy loss in PSII) of R. rugosa in the coastal sand dune, they dissipated the excessed photon energy through the non-photochemical quenching (NPQ) mechanism when they were exposed to relatively low PAR and low temperature. Rosa rugosa in the coastal sand dune has higher chlorophyll a and carotenoid content. The high chlorophyll a + b and low chlorophyll a/b ratios seemed to optimize light absorption in response to low PAR. High carotenoid content played an important role in NPQ. As a part of the osmotic regulation in response to low LWCs, R. rugosa exposed to high temperatures and continuously high PAR used soluble carbohydrates and ions to maintain high osmolality. Conclusions: We found that Fv/Fm was lower in the potted plants than in the coastal sand dune plants, indicating the vulnerability of R. rugosa to high temperatures and PAR levels. We expect that the suitable habitat range for R. rugosa will shrink and move to north under climate change conditions.

Keywords

Acknowledgement

All the authors are deeply grateful to plant ecophysiology lab in Kyungpook National University, Republic of Korea.

References

  1. Adams SR, Langton FA. Photoperiod and plant growth: a review. J Hortic Sci Biotechnol. 2005;80(1):2-10. https://doi.org/10.1080/14620316.2005.11511882.
  2. Adams WW 3rd, Demmig-Adams B, Logan BA, Barker DH, Osmond CB. Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understory of an open Eucalyptus forest. Plant Cell Environ. 1999;22(2):125-36. https://doi.org/10.1046/j.1365-3040.1999.00369.x.
  3. Albanese P, Tamara S, Saracco G, Scheltema RA, Pagliano C. How paired PSII-LHCII supercomplexes mediate the stacking of plant thylakoid membranes unveiled by structural mass-spectrometry. Nat Commun. 2020;11(1):1361. https://doi.org/10.1038/s41467-020-15184-1.
  4. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P. Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res. 2008;98(1-3):541-50. https://doi.org/10.1007/s11120-008-9331-0.
  5. Allen JF, de Paula WB, Puthiyaveetil S, Nield J. A structural phylogenetic map for chloroplast photosynthesis. Trends Plant Sci. 2011;16(12):645-55. https://doi.org/10.1016/j.tplants.2011.10.004.
  6. Anderson MC. Photon flux, chlorophyll content, and photosynthesis under natural conditions. Ecology. 1967;48(6):1050-3. https://doi.org/10.2307/1934566.
  7. Aro EM, McCaffery S, Anderson JM. Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol. 1993a;103(3):835-43. https://doi.org/10.1104/pp.103.3.835.
  8. Aro EM, Virgin I, Andersson B. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta. 1993b;1143(2):113-34. https://doi.org/10.1016/0005-2728(93)90134-2.
  9. Ashraf M, Harris PJC. Photosynthesis under stressful environments: an overview. Photosynthetica. 2013;51(2):163-90. https://doi.org/10.1007/s11099-013-0021-6.
  10. Ball MC, Cowan IR, Farquhar GD. Maintenance of leaf temperature and the optimisation of carbon gain in relation to water loss in a tropical mangrove forest. Funct Plant Biol. 1988;15(2):263-76. https://doi.org/10.1071/PP9880263.
  11. Billings WD. The environmental complex in relation to plant growth and distribution. Q Rev Biol. 1952;27(3):251-65. https://doi.org/10.1086/399022.
  12. Blum A. Drought resistance, water-use efficiency, and yield potential-are they compatible, dissonant, or mutually exclusive? Aust J Agric Res. 2005;56(11):1159-68. https://doi.org/10.1071/AR05069.
  13. Bozarth CS, Kennedy RA, Schekel KA. The effects of leaf age on photosynthesis in rose1. J Am Soc Hortic Sci. 1982;107(5):707-12. https://doi.org/10.21273/JASHS.107.5.707.
  14. Chang B, Ma K, Lu Z, Lu J, Cui J, Wang L, et al. Physiological, transcriptomic, and metabolic responses of Ginkgo biloba L. to drought, salt, and heat stresses. Biomolecules. 2020;10(12):1635. https://doi.org/10.3390/biom10121635.
  15. Chapin FS 3rd, Schulze E, Mooney HA. The ecology and economics of storage in plants. Annu Rev Ecol Syst. 1990;21(1):423-47. https://doi.org/10.1146/annurev.es.21.110190.002231.
  16. Chen JW, Kuang SB, Long GQ, Yang SC, Meng ZG, Li LG, et al. Photosynthesis, light energy partitioning, and photoprotection in the shade-demanding species Panax notoginseng under high and low level of growth irradiance. Funct Plant Biol. 2016;43(6):479-91. https://doi.org/10.1071/fp15283.
  17. Choi YH, Kim MJ, Lee HS, Hu C, Kwak SS. Antioxidants in leaves of Rosa rugose. Korean J Pharmacogn. 1997;28(4):179-84.
  18. Dai Y, Shen Z, Liu Y, Wang L, Hannaway D, Lu H. Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot. 2009;65(2-3):177-82. https://doi.org/10.1016/j.envexpbot.2008.12.008.
  19. Dale MP, Causton DR. Use of the chlorophyll a/b ratio as a bioassay for the light environment of a plant. Funct Ecol. 1992;6(2):190-6. https://doi.org/10.2307/2389754.
  20. Demmig-Adams B, Adams WW 3rd. Photoprotection and other responses of plants to high light stress. Annu Rev Plant Biol. 1992;43:599-626. https://doi.org/10.1146/annurev.pp.43.060192.003123.
  21. Demmig-Adams B. Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol. 1998;39(5):474-82. https://doi.org/10.1093/oxfordjournals.pcp.a029394.
  22. dos Santos TB, Ribas AF, de Souza SGH, Budzinski IGF, Domingues DS. Physiological responses to drought, salinity, and heat stress in plants: a review. Stresses. 2022;2(1):113-35. https://doi.org/10.3390/stresses2010009.
  23. Fedotova MV. Compatible osmolytes - bioprotectants: is there a common link between their hydration and their protective action under abiotic stresses? J Mol Liq. 2019;292:111339. https://doi.org/10.1016/j.molliq.2019.111339.
  24. Flowers TJ, Yeo AR. Ion relations of plants under drought and salinity. Funct Plant Biol. 1986;13(1):75-91. https://doi.org/10.1071/PP9860075.
  25. Frosini S, Lardicci C, Balestri E. Global change and response of coastal dune plants to the combined effects of increased sand accretion (burial) and nutrient availability. PLoS One. 2012;7(10):e47561. https://doi.org/10.1371/journal.pone.0047561.
  26. Gates DM. Leaf temperature and transpiration1. Agron J. 1964;56(3):273-7. https://doi.org/10.2134/agronj1964.00021962005600030007x.
  27. Gil R, Boscaiu M, Lull C, Bautista I, Lid N A, Vicente O. Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct Plant Biol. 2013;40(9):805-18. https://doi.org/10.1071/fp12359.
  28. Gilmore AM. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant. 1997;99(1):197-209. https://doi.org/10.1111/j.1399-3054.1997.tb03449.x.
  29. Girija C, Smith BN, Swamy PM. Interactive effects of sodium chloride and calcium chloride on the accumulation of proline and glycinebetaine in peanut (Arachis hypogaea L.). Environ Exp Bot. 2002;47(1):1-10. https://doi.org/10.1016/S0098-8472(01)00096-X.
  30. Givnish TJ. Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constraints. New Phytol. 1987;106(s1):131-60. https://doi.org/10.1111/j.1469-8137.1987.tb04687.x.
  31. Han YH, Lee YH, Kim JB, Cho KJ. Vegetation characteristics of coastal sand dune in the East Coast. J Korean Soc Environ Restor Technol. 2013;16(1):55-69. https://doi.org/10.13087/KOSERT.2013.16.1.055.
  32. Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci. 2013;14(5):9643-84. https://doi.org/10.3390/ijms14059643.
  33. Hatfield JL, Dold C. Water-use efficiency: advances and challenges in a changing climate. Front Plant Sci. 2019;10:103. https://doi.org/10.3389/fpls.2019.00103.
  34. Hessini K, Martinez JP, Gandour M, Albouchi A, Soltani A, Abdelly C. Effect of water stress on growth, osmotic adjustment, cell wall elasticity and water-use efficiency in Spartina alterniflora . Environ Exp Bot. 2009;67(2):312-9. https://doi.org/10.1016/j.envexpbot.2009.06.010.
  35. Hohmann-Marriott MF, Blankenship RE. Evolution of photosynthesis. Annu Rev Plant Biol. 2011;62:515-48. https://doi.org/10.1146/annurev-arplant-042110-103811.
  36. Hu S, Ding Y, Zhu C. Sensitivity and responses of chloroplasts to heat stress in plants. Front Plant Sci. 2020;11:375. https://doi.org/10.3389/fpls.2020.00375.
  37. Iyer NJ, Tang Y, Mahalingam R. Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant Cell Environ. 2013;36(3):706-20. https://doi.org/10.1111/pce.12008.
  38. Jahnke LS, Hull MR, Long SP. Chilling stress and oxygen metabolizing enzymes in Zea mays and Zea diploperennis . Plant Cell Environ. 1991;14(1):97-104. https://doi.org/10.1111/j.1365-3040.1991.tb01375.x.
  39. Jensen PE, Leister D. Chloroplast evolution, structure and functions. F1000Prime Rep. 2014;6:40. https://doi.org/10.12703/p6-40.
  40. Jiang Y, Wang XX, Meng H, Xu YW, Wang S, Wang SD. Photosynthetic physiology performance and expression of transcription factors in soybean of water use efficiency difference. Russ J Plant Physiol. 2022;69(1):9. https://doi.org/10.1134/S102144372201006X.
  41. Joung YH, Kim ST, Kim GJ, Lee JH, Gi GY, Han TH. Genetic relationship of genus Rosa germplasm and genetic diversity of Rosa rugosa in Korea. Korean J Hortic Sci Technol. 2010;28(6):1003-13.
  42. Kappel F, Flore JA. Effect of shade on photosynthesis, specific leaf weight, leaf chlorophyll content, and morphology of young peach trees. J Am Soc Hortic Sci. 1983;108(4):541-4. https://doi.org/10.21273/JASHS.108.4.541.
  43. Kawakami K, Shen JR. Purification of fully active and crystallizable photosystem II from thermophilic cyanobacteria. Methods Enzymol. 2018;613:1-16. https://doi.org/10.1016/bs.mie.2018.10.002.
  44. Kim MJ, Kim JS, Kim KE, Shin KH, Heo K, Cho DH, et al. Comparison of antioxidative activities from different organs of Rosa rugosa Thunb. Korean J Med Crop Sci. 2001;9(1):40-4.
  45. Kitao M, Lei TT, Koike T, Tobita H, Maruyama Y. Susceptibility to photoinhibition of three deciduous broadleaf tree species with different successional traits raised under various light regimes. Plant Cell Environ. 2000;23(1):81-9. https://doi.org/10.1046/j.1365-3040.2000.00528.x.
  46. Larkindale J, Huang B. Changes of lipid composition and saturation level in leaves and roots for heat-stressed and heat-acclimated creeping bentgrass (Agrostis stolonifera). Environ Exp Bot. 2004;51(1):57-67. https://doi.org/10.1016/S0098-8472(03)00060-1.
  47. Lee JY, Lee JH, Ki GY, Kim ST, Han TH. Improvement of seed germination in Rosa rugosa. Korean J Hortic Sci Technol. 2011;29(4):352-7.
  48. Long SP, Humphries S, Falkowski PG. Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol. 1994;45(1):633-62. https://doi.org/10.1146/annurev.pp.45.060194.003221.
  49. Lu T, Meng Z, Zhang G, Qi M, Sun Z, Liu Y, et al. Sub-high temperature and high light intensity induced irreversible inhibition on photosynthesis system of tomato plant (Solanum lycopersicum L.). Front Plant Sci. 2017;8:365. https://doi.org/10.3389/fpls.2017.00365.
  50. Medina E, Francisco M. Osmolality and δ13C of leaf tissues of mangrove species from environments of contrasting rainfall and salinity. Estuar Coast Shelf Sci. 1997;45(3):337-44. https://doi.org/10.1006/ecss.1996.0188.
  51. Munns R, Brady CJ, Barlow EWR. Solute accumulation in the apex and leaves of wheat during water stress. Funct Plant Biol. 1979;6(3):379-89. https://doi.org/10.1071/PP9790379.
  52. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta. 2007;1767(6):414-21. https://doi.org/10.1016/j.bbabio.2006.11.019.
  53. National Institute of Ecology. Floristic Target Species (FT Species) in Korea. Seocheon: National Institute of Ecology; 2018.
  54. Parkhill JP, Maillet G, Cullen JJ. Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol. 2001;37(4):517-29. https://doi.org/10.1046/j.1529-8817.2001.037004517.x.
  55. Pazur JH. Neutral polysaccharide. In: Chaplin MF, Kennedy JF, editors. Carbohydrate analysis: a practical approach. 2nd ed. Oxford: IRL Press; 1994. p. 90-2.
  56. Pfundel E, Klughammer C, Schreiber U. Monitoring the effects of reduced PS II antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system. PAM Appl Notes. 2008;1:21-4.
  57. Prasch CM, Sonnewald U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 2013;162(4):1849-66. https://doi.org/10.1104/pp.113.221044.
  58. Rajaniemi TK, Allison VJ. Abiotic conditions and plant cover differentially affect microbial biomass and community composition on dune gradients. Soil Biol Biochem. 2009;41(1):102-9. https://doi.org/10.1016/j.soilbio.2008.10.001.
  59. Rajkumar M, Bruno LB, Banu JR. Alleviation of environmental stress in plants: the role of beneficial Pseudomonas spp. Crit Rev Environ Sci Technol. 2017;47(6):372-407. https://doi.org/10.1080/10643389.2017.1318619.
  60. Ruban AV. Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol. 2016;170(4):1903-16. https://doi.org/10.1104/pp.15.01935.
  61. Sharma DK, Andersen SB, Ottosen CO, Rosenqvist E. Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiol Plant. 2015;153(2):284-98. https://doi.org/10.1111/ppl.12245.
  62. Shin WS, Lee B, Jeong B, Chang YK, Kwon JH. Truncated light-harvesting chlorophyll antenna size in Chlorella vulgaris improves biomass productivity. J Appl Phycol. 2016;28(6):3193-202. https://doi.org/10.1007/s10811-016-0874-8.
  63. Silva EN, Vieira SA, Ribeiro RV, Ponte LFA, Ferreira-Silva SL, Silveira JAG. Contrasting physiological responses of Jatropha curcas plants to single and combined stresses of salinity and heat. J Plant Growth Regul. 2013;32(1):159-69. https://doi.org/10.1007/s00344-012-9287-3.
  64. Sinclair TR, Tanner CB, Bennett JM. Water-use efficiency in crop production. BioScience. 1984;34(1):36-40. https://doi.org/10.2307/1309424.
  65. Singh J, Thakur JK. Photosynthesis and abiotic stress in plants. In: Vats S, editor. Biotic and abiotic stress tolerance in plants. Singapore: Springer; 2018. p. 27-46.
  66. Stanhill G. Water use efficiency. Adv Agron. 1986;39:53-85. https://doi.org/10.1016/S0065-2113(08)60465-4.
  67. Sudhir P, Murthy SDS. Effects of salt stress on basic processes of photosynthesis. Photosynthetica. 2004;42(4):481-6. https://doi.org/10.1007/S11099-005-0001-6.
  68. Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. Abiotic and biotic stress combinations. New Phytol. 2014;203(1):32-43. https://doi.org/10.1111/nph.12797.
  69. Taiz L, Zeiger E. Plant physiology. 5th ed. Sunderland: Sinauer Associates is an imprint of Oxford University Press; 2010.
  70. Takahashi S, Badger MR. Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci. 2011;16(1):53-60. https://doi.org/10.1016/j.tplants.2010.10.001.
  71. Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 2008;13(4):178-82. https://doi.org/10.1016/j.tplants.2008.01.005.
  72. Tanaka R, Koshino Y, Sawa S, Ishiguro S, Okada K, Tanaka A. Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana. Plant J. 2001;26(4):365-73. https://doi.org/10.1046/j.1365-313x.2001.2641034.x.
  73. Thakur P, Nayyar H. Facing the cold stress by plants in the changing environment: sensing, signaling, and defending mechanisms. In: Tuteja N, Gill SS, editors. Plant acclimation to environmental stress. New York: Springer; 2013. p. 29-69. https://doi.org/10.1007/978-1-4614-5001-6_2
  74. Tyystjarvi E. Photoinhibition of photosystem II. Int Rev Cell Mol Biol. 2013;300:243-303. https://doi.org/10.1016/b978-0-12-405210-9.00007-2.
  75. Vicente O, Al Hassan M, Boscaiu M. Contribution of osmolyte accumulation to abiotic stress tolerance in wild plants adapted to different stressful environments. In: Iqbal N, Nazar R, Khan NA, editors. Osmolytes and plants acclimation to changing environment: emerging omics technologies. New Delhi: Springer; 2016. p. 13-25.
  76. Villar R, Robleto JR, De Jong Y, Poorter H. Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant Cell Environ. 2006 Aug;29(8):1629-43. https://doi.org/10.1111/j.1365-3040.2006.01540.x.
  77. Wang F, Zhang F, Gou X, Fonti P, Xia J, Cao Z, et al. Seasonal variations in leaf-level photosynthesis and water use efficiency of three isohydric to anisohydric conifers on the Tibetan Plateau. Agric For Meteorol 2021;308-309:108581. https://doi.org/10.1016/j.agrformet.2021.108581.
  78. Weis E, Berry JA. Quantum efficiency of Photosystem II in relation to 'energy'-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta Bioenerg. 1987;894(2):198-208. https://doi.org/10.1016/0005-2728(87)90190-3.
  79. Wellburn AR. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physio. 1994;144(3):307-13. https://doi.org/10.1016/S0176-1617(11)81192-2.
  80. Wittmann C, Aschan G, Pfanz H. Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regime. Basic Appl Ecol. 2001:2(2):145-54. https://doi.org/10.1078/1439-1791-00047.
  81. Yamori W, Hikosaka K, Way DA. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res. 2014;119(1-2):101-17. https://doi.org/10.1007/s11120-013-9874-6.
  82. Young HS. Antihypertensive activity and triterpene from the underground parts of Rosa rugose. J Oriental Bot Res 1990;3(2):83-9.
  83. Yu HS, Mun YJ, Woo WH, Song JH. Anti-melanogenic effects of ethanol extracts from Rosa rugosa thunb. J Korean Soc Cosmetol. 2014;20(1):36-41.
  84. Zhang Y, He N, Yu G. Opposing shifts in distributions of chlorophyll concentration and composition in grassland under warming. Sci Rep. 2021;11(1):15736. https://doi.org/10.1038/s41598-021-95281-3.