Photosynthetica 2020, 58(5):1226-1236 | DOI: 10.32615/ps.2020.073

Effect of drought and heat stresses on photosynthesis, pigments, and xanthophyll cycle in alfalfa (Medicago sativa L.)

C. XU1,2,†, C.G. HE1,†, Y.J. WANG1, Y.F. BI1, H. JIANG1
1 College of Animal Sciences and Technology, Yunnan Agricultural University, Kunming, Yunnan, China
2 Kunming Agricultural Radio and Television School, Kunming, Yunnan, China

Climate changes severely influence photosynthetic activity of plants. Studies on the combined effect of drought and heat stress on photosynthesis, pigments, and xanthophyll cycle particularly in alfalfa (Medicago sativa L.) are limited. Thus, this study investigated the combined effects of drought and heat stress in two alfalfa varieties ('Deqin' and 'Algonguin'). Results revealed that the values of the net photosynthetic rate demonstrated a significantly decreasing tendency under stresses. The effect of stresses on ribulose 1,5-bisphosphate carboxylase activity in both varieties showed a trend of first declining and then rising. Meanwhile, phosphoenolpyruvate carboxylase activity showed an increasing tendency. The intensification of stresses led to reduced photochemical efficiency and increased capability of thermal dissipation. A linear correlation was found between nonphotochemical quenching and xanthophyll cycle components. Thus, the change in carotenoids demonstrated an important role in photoprotection, the xanthophyll cycle was the main way of dissipation of excess energy under stress conditions in alfalfa.

Additional key words: abiotic stress; global warming; photosynthetic parameters; thermal dissipation.

Received: July 3, 2020; Revised: September 7, 2020; Accepted: October 14, 2020; Prepublished online: November 16, 2020; Published: December 8, 2020  Show citation

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XU, C., HE, C.G., WANG, Y.J., BI, Y.F., & JIANG, H. (2020). Effect of drought and heat stresses on photosynthesis, pigments, and xanthophyll cycle in alfalfa (Medicago sativa L.). Photosynthetica58(5), 1226-1236. doi: 10.32615/ps.2020.073
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References

  1. Alonso R., Elvira S., Castillo F.J., Gimeno B.S.: Interactive effects of ozone and drought stress on pigments and activities of antioxidative enzymes in Pinus halepensis. - Plant Cell Environ. 24: 905-916, 2001. Go to original source...
  2. Aranjuelo I., Irigoyen J.J., Sánchez-Díaz M.: Effect of elevated temperature and water availability on CO2 exchange and nitrogen fixation of nodulated alfalfa plants. - Environ. Exp. Bot. 59: 99-108, 2007. Go to original source...
  3. Ashida H., Danchin A., Yokota A.: Was photosynthetic RuBisCO recruited by acquisitive evolution from RuBisCO-like proteins involved in sulfur metabolism? - Res. Microbiol. 156: 611-618, 2005. Go to original source...
  4. Bi Y.F., Che W.G., Gu L.: [Polymorphic characteristics and origin analysis of wild alfalfa population (Medicago sativa L.) in Deqin area.] - Acta Agr. Sin. 15: 306-311, 2007. [In Chinese] doi: 10.11733/j.issn.1007-0435.2007.04.002. Go to original source...
  5. Biswas D.K., Ma B.L., Xu H. et al.: Lutein-mediated photo-protection of photosynthetic machinery in Arabidopsis thaliana exposed to chronic low ultraviolet-B radiation. - J. Plant Physiol. 248: 153160, 2020. Go to original source...
  6. Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. - Ann. Bot.-London 103: 551-560, 2009. Go to original source...
  7. D.M., Antunes W.C., Pinheiro D.P. et al.: Tobacco guard cells fix CO2 by both Rubisco and PEPcase while sucrose acts as a substrate during light-induced stomatal opening. - Plant Cell Environ. 38: 2353-2371, 2015.
  8. Das A., Eldakak M., Paudel B. et al.: Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. - Biomed Res. Int. 2016: 6021047, 2016. Go to original source...
  9. Demmig-Adams B.: Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. - BBA-Bioenergetics 1020: 1-24, 1990. Go to original source...
  10. Demmig-Adams B., Adams III W.W.: Photoprotection and other responses of plants to high light stress. - Annu. Rev. Plant Phys. 43: 599-626, 1992. Go to original source...
  11. Dhami N., Drake J.E., Tjoelker M.G. et al.: An extreme heatwave enhanced the xanthophyll de-epoxidation state in leaves of Eucalyptus trees grown in the field. - Physiol. Mol. Biol. Pla. 26: 211-218, 2020. Go to original source...
  12. Eskling M., Arvidsson P.-O., Åkerlund H.-E.: The xanthophyll cycle, its regulation and components. - Physiol. Plantarum 100: 806-816, 1997. Go to original source...
  13. Flexas J., Bota J., Loreto F. et al.: Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. - Plant Biol. 6: 269-279, 2004. Go to original source...
  14. Flexas J., Medrano H.: Drought-inhibition of photosynthesis in C3 plants: Stomatal and non-stomatal limitations revisited. - Ann. Bot.-London 89: 183-189, 2002. Go to original source...
  15. Flexas J., Ribas-Carbó M., Bota J. et al.: Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. - New Phytol. 172: 73-82, 2006. Go to original source...
  16. Frank H.A., Bautista J.A., Josue J.S., Young A.J.: Mechanism of nonphotochemical quenching in green plants: Energies of the lowest excited singlet states of violaxanthin and zeaxanthin. - Biochemistry-US 39: 2831-2837, 2000. Go to original source...
  17. Furumoto T., Izui K., Quinn V. et al.: Phosphorylation of phosphoenolpyruvate carboxylase is not essential for high photosynthetic rates in the C4 species Flaveria bidentis. - Plant Physiol. 144: 1936-1945, 2007. Go to original source...
  18. Gallego-Tévar B., Peinado-Torrubia P., Álvarez R. et al.: From physiology to salt marsh management challenges with sea level rise: the case of native Spartina foliosa, invasive S. densiflora and their hybrid. - Conserv. Physiol. 8: coaa053, 2020a. Go to original source...
  19. Gallego-Tévar B., Peinado-Torrubia P., Álvarez R. et al.: Changes to the functional traits of phosphoenolpyruvate carboxylase following hybridization in C-4 halophytes. - Physiol. Plantarum 169: 83-98, 2020b. Go to original source...
  20. Gao S., Su P.X., Yan Q.D., Ding S.S.: Canopy and leaf gas exchange of Haloxylon ammodendron under different soil moisture regimes. - Sci. China Life Sci. 53: 718-728, 2010. Go to original source...
  21. García-Mauriño S., Monreal J., Alvarez R. et al.: Characterization of salt stress-enhanced phosphoenolpyruvate carboxylase kinase activity in leaves of Sorghum vulgare: independence from osmotic stress, involvement of ion toxicity and significance of dark phosphorylation. - Planta 216: 648-655, 2003. Go to original source...
  22. Gerganova M., Popova A.V., Stanoeva D., Velitchkova M.: Tomato plants acclimate better to elevated temperature and high light than to treatment with each factor separately. - Plant Physiol. Bioch. 104: 234-241, 2016. Go to original source...
  23. Gilmore A.M.: Xanthophyll cycle-dependent nonphotochemical quenching in photosystem II: Mechanistic insights gained from Arabidopsis thaliana L. mutants that lack violaxanthin deepoxidase activity and/or lutein. - Photosynth. Res. 67: 89-101, 2001. Go to original source...
  24. Gilmore A.M., Yamamoto H.Y.: Linear models relating xantho-phylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. - Photosynth. Res. 35: 67-78, 1993. Go to original source...
  25. Gong D.H., Wang G.Z., Si W.T. et al.: Effects of salt stress on photosynthetic pigments and activity of ribulose-1,5-bisphosphate carboxylase/oxygenase in Kalidium foliatum. - Russ. J. Plant Physl+ 65: 98-103, 2018. Go to original source...
  26. Greer D.H., Weedon M.M.: Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate. - Plant Cell Environ. 35: 1050-1064, 2012. Go to original source...
  27. Guo D.P., Guo Y.P., Zhao J.P. et al.: Photosynthetic rate and chlorophyll fluorescence in leaves of stem mustard (Brassica juncea var. tsatsai) after turnip mosaic virus infection. - Plant Sci. 168: 57-63, 2005. Go to original source...
  28. Hao L., Wang Y., Zhang J. et al.: Coronatine enhances drought tolerance via improving antioxidative capacity to maintaining higher photosynthetic performance in soybean. - Plant Sci. 210: 1-9, 2013. Go to original source...
  29. Hassanzadeh M., Ebadi A., Panahyan-e-Kivi M. et al.: Evaluation of drought stress on relative water content and chlorophyll content of sesame (Sesamum indicum L.) genotypes at early flowering stage. - Res. J. Environ. Sci. 3: 345-350, 2009. Go to original source...
  30. Hinojosa L., Sanad M.N.M.E., Jarvis D.E. et al.: Impact of heat and drought stress on peroxisome proliferation in quinoa. - Plant J. 99: 1144-1158, 2019. Go to original source...
  31. Honoki R., Ono S., Oikawa A. et al.: Significance of accumulation of the alarmone (p)ppGpp in chloroplasts for controlling photosynthesis and metabolite balance during nitrogen starvation in Arabidopsis. - Photosynth. Res. 135: 299-308, 2018. Go to original source...
  32. IPCC 2014: Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Pp. 151. IPCC, Geneva 2014.
  33. Jiang Y.W., Huang B.R.: Physiological responses to heat stress alone or in combination with drought: A comparison between tall fescue and perennial ryegrass. - HortScience 36: 682-686, 2001. Go to original source...
  34. Johnson M.P., Davison P.A., Ruban A.V., Horton P.: The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. - FEBS Lett. 582: 262-266, 2008. Go to original source...
  35. Lawlor D.W., Cornic G.: Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. - Plant Cell Environ. 25: 275-294, 2002. Go to original source...
  36. Lawlor D.W., Tezara W.: Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: A critical evaluation of mechanisms and integration of processes. - Ann. Bot.-London 103: 561-579, 2009. Go to original source...
  37. León-Sánchez L., Nicolás E., Prieto I. et al.: Altered leaf elemental composition with climate change is linked to reductions in photosynthesis, growth and survival in a semi-arid shrubland. - J. Ecol. 108: 47-60, 2020. Go to original source...
  38. Li H.S.: [Determination of the activity of ribulose 1,5-bisphosphate carboxylase.] - In: Li H.S. (ed.): [The Experimental Principle and Technology in the Plant Physiology and Biochemistry.] Pp. 138-142. Higher Education Press, Beijing 2000. [In Chinese]
  39. Li R., Wang Y.J., He C.G. et al.: [Effect of drought and heat stress on morphology and photosynthetic pigment contents of Medicago sativa.] - Grassl. T. 35: 37-43, 2015. [In Chinese] doi: 10.13817/j.cnki.cyycp.2015.01.007. Go to original source...
  40. Liang G., Bu J., Zhang S. et al.: Effects of drought stress on the photosynthetic physiological parameters of Populus × euramericana 'Neva'. - J. Forestry Res. 30: 409-416, 2019. Go to original source...
  41. Liguori N., Croce R., Marrink S.J., Thallmair S.: Molecular dynamics simulations in photosynthesis. - Photosynth. Res. 144: 273-295, 2020. Go to original source...
  42. Liu C., Liu Y., Guo K. et al.: Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. - Environ. Exp. Bot. 71: 174-183, 2011. Go to original source...
  43. Liu J., Guo Y.Y., Bai Y.W. et al.: Effects of drought stress on the photosynthesis in maize. - Russ. J. Plant Physl+ 65: 849-856, 2018. Go to original source...
  44. Lu Q., Lu C., Zhang J., Kuang T.: Photosynthesis and chlorophyll a fluorescence during flag leaf senescence of field-grown wheat plants. - J. Plant Physiol. 159: 1173-1178, 2002. Go to original source...
  45. Lundqvist T., Schneider G.: Crystal structure of activated ribulose-1,5-bisphosphate carboxylase complexed with its substrate, ribulose-1,5-bisphosphate. - J. Biol. Chem. 266: 12604-12611, 1991. Go to original source...
  46. Ma X.L., Bi Y.F.: [Isozyme studies on polyphenol oxidase and superoxide dismutase of wide and escaped alfalfa germplasm resources in Yunnan.] - Acta Agr. Sin. 19: 509-515, 2011. [In Chinese] doi: 10.11733/j.issn.1007-0435.2011.03.026. Go to original source...
  47. Majumdar S., Ghosh S., Glick B.R., Dumbroff E.B.: Activities of chlorophyllase, phosphoenolpyruvate carboxylase and ribulose-1,5-bisphosphate carboxylase in the primary leaves of soybean during senescence and drought. - Physiol. Plantarum 81: 473-480, 1991. Go to original source...
  48. Morales F., Ancín M., Fakhet D. et al.: Photosynthetic metabolism under stressful growth conditions as a bases for crop breeding and yield improvement. - Plants-Basel 9: 88, 2020. Go to original source...
  49. Mu L., He C.G., Jiang H. et al.: [The effects of drought and heat stress on the photosynthetic characteristics of alfalfa.] - Acta Agr. Sin. 22: 550-555, 2014. [In Chinese] doi: 10.11733/j.issn.1007-0435.2014.03.017. Go to original source...
  50. Najar R., Aydi S., Sassi-Aydi S. et al.: Effect of salt stress on photosynthesis and chlorophyll fluorescence in Medicago truncatula. - Plant Biosyst. 153: 88-97, 2019. Go to original source...
  51. Panković D., Sakač Z., Kevreąan S., Plesničar M.: Acclimation to long-term water deficit in the leaves of two sunflower hybrids: photosynthesis, electron transport and carbon metabolism. - J. Exp. Bot. 50: 128-138, 1999. Go to original source...
  52. Parry M.A.J., Andralojc P.J., Khan S. et al.: Rubisco activity: Effects of drought stress. - Ann. Bot.-London 89: 833-839, 2002. Go to original source...
  53. Pfündel E., Bilger W.: Regulation and possible function of the violaxanthin cycle. - Photosynth. Res. 42: 89-109, 1994. Go to original source...
  54. Rai R., Agrawal M., Agrawal S.B.: Effects of ambient O3 on wheat during reproductive development: Gas exchange, photosynthetic pigments, chlorophyll fluorescence, and carbohydrates. - Photosynthetica 49: 285-294, 2011. Go to original source...
  55. Redondo-Gómez S., Mateos-Naranjo E., Davy A.J. et al.: Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. - Ann. Bot.-London 100: 555-563, 2007. Go to original source...
  56. Rizhsky L., Liang H.J., Mittler R.: The combined effect of drought stress and heat shock on gene expression in tobacco. -Plant Physiol. 130: 1143-1151, 2002. Go to original source...
  57. Rizhsky L., Liang H.J., Mittler R.: When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. - Plant Physiol. 134: 1683-1696, 2004. Go to original source...
  58. Sánchez-Rodríguez J., Pérez P., Martínez-Carrasco R.: Photosyn-thesis, carbohydrate levels and chlorophyll fluorescence-estimated intercellular CO2 in water stressed Casuarina equisetifolia Forst. & Forst. - Plant Cell Environ. 22: 867-873, 1999. Go to original source...
  59. Sattar A., Sher A., Ijaz M. et al.: Terminal drought and heat stress alter physiological and biochemical attributes in flag leaf of bread wheat. - PLoS ONE 15: e0232974, 2020. Go to original source...
  60. Sehgal A., Sita K., Kumar J. et al.: Effects of drought, heat and their interaction on the growth, yield and photosynthetic function of lentil (Lens culinaris Medikus) genotypes varying in heat and drought sensitivity. - Front. Plant Sci. 8: 1776, 2017. Go to original source...
  61. Tang L., Cai H., Zhai H. et al.: Overexpression of Glycine soja WRKY20 enhances both drought and salt tolerance in transgenic alfalfa (Medicago sativa L.). - Plant Cell Tiss. Org. 118: 77-86, 2014. Go to original source...
  62. Tewari A.K., Tripathy B.C.: Temperature-stress-induced impair-ment of chlorophyll biosynthetic reactions in cucumber and wheat. - Plant Physiol. 117: 851-858, 1998. Go to original source...
  63. Tzortzakis N., Chrysargyris A., Aziz A.: Adaptive response of a native Mediterranean grapevine cultivar upon short-term exposure to drought and heat stress in the context of climate change. - Agronomy 10: 249, 2020. Go to original source...
  64. Vieira E.A., Silva M.D.G., Moro C.F., Laura V.A.: Physiological and biochemical changes attenuate the effects of drought on the Cerrado species Vatairea macrocarpa (Benth.) Ducke. - Plant Physiol. Bioch. 115: 472-483, 2017. Go to original source...
  65. Wang Y.J., Jiang H., Bi Y.F., Zhao F.: [Photosynthesis physiological response to dry-hot environment in alfalfa.] -J. Yunnan Agr. Univ. 26: 90-193, 2011. [In Chinese] doi: 10.3969/j.issn.1004-390X(n).2011.02.008. Go to original source...
  66. Wassie M., Zhang W., Zhang Q. et al.: Effect of heat stress on growth and physiological traits of alfalfa (Medicago sativa L.) and a comprehensive evaluation for heat tolerance. - Agronomy 9: 597, 2019. Go to original source...
  67. Wei C.L., Jiang C.J., Tao H.Z.: [Analysis of the xanthophyll leaves of tea plant by high cycle component in fresh chroma-tography and its performance liquid photoprotection.] - J. Tea Sci. 24: 60-64, 2004. [In Chinese] doi: 10.3969/j.issn.1000-369X.2004.01.012. Go to original source...
  68. Weng X.Y., Xu H.X., Jiang D.A.: Characteristics of gas exchange, chlorophyll fluorescence and expression of key enzymes in photosynthesis during leaf senescence in rice plants. - J. Integr. Plant Biol. 47: 560-566, 2005. Go to original source...
  69. Xu C., He C.G., Duan X.H. et al.: [Determining the content of xanthophyll cycle components in alfalfa leaves by HPLC.] -J. Yunnan Agr. Univ. 34: 820-825, 2019. [In Chinese] doi: 10.12101/j.issn.1004-390X(n).201904083. Go to original source...
  70. You L., Zhang Y., Li L. et al.: Involvement of abscisic acid, ABI5, and PPC2 in plant acclimation to low CO2. - J. Exp. Bot. 71: 4093-4108, 2020. Go to original source...
  71. Yu M.H., Mao Z.C., Ye S.H.: [Determination of chloroplast pigment content (spectrophotometric method).] - In: Ye S.H. (ed.): [Plant Physiology and Biochemistry Eperiment Course.] Pp. 116-119. Yunnan Science and Technology Press, Yunnan 2004. [In Chinese]
  72. Zhang Q., Liu X., Zhang Z. et al.: Melatonin improved waterlogging tolerance in alfalfa (Medicago sativa) by reprogramming polyamine and ethylene metabolism. - Front. Plant Sci. 10: 44, 2019. Go to original source...
  73. Zhang Z., Wang Y., Chang L. et al.: MsZEP, a novel zeaxanthin epoxidase gene from alfalfa (Medicago sativa), confers drought and salt tolerance in transgenic tobacco. - Plant Cell Rep. 35: 439-453, 2016. Go to original source...
  74. Zhao Y., Guo A., Wang Y., Hua J.: Evolution of PEPC gene family in Gossypium reveals functional diversification and GhPEPC genes responding to abiotic stresses. - Gene 698: 61-71, 2019. Go to original source...
  75. Zhao Y.L., Xiong H., Bi Y.F. et al.: [Effect of drought and heat stress on leaf stomata size in alfalfa.] - J. Yunnan Agr. Univ. 28: 336-339, 2013. [In Chinese] doi: 10.3969/j.issn.1004-390X(n).2013.03.009. Go to original source...
  76. Zhou R., Yu X., Ottosen C.-O. et al.: Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. - BMC Plant Biol. 17: 24, 2017. Go to original source...