Photosynthetica 2019, 57(1):86-95 | DOI: 10.32615/ps.2019.001

Role of arbuscular mycorrhiza in alleviating the effect of cold on the photosynthesis of cucumber seedlings

J. MA1,2, M. JANOUŠKOVÁ3, L. YE1, L.Q. BAI2, R.R. DONG2, Y. YAN2, X.C. YU2, Z.R. ZOU1, Y.S. LI2, C.X. HE2
1 College of Grain Engineering, Food & Drug, Jiangsu Vocational College of Finance & Economics, Huaian, Jiangsu 223001, China
2 Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China
3 Institute of Botany, Academy of Sciences of the Czech Republic, Pruhonice 25243, Czech Republic

Arbuscular mycorrhiza (AM) is known to enhance the rate of photosynthesis in plants, but there is little information on whether this effect is maintained at low temperature when the development of AM fungi is restrained. We therefore investigated the influence of AM on gas exchange, PSII fluorescence, and some photosynthesis-related biochemical parameters in cucumber seedlings under cold stress. Cold stress decreased, as expected, the chlorophyll content, net photosynthetic rate, and parameters related to photochemical quenching, while increasing nonphotochemical quenching and sugar contents in leaves. In contrast, AM had opposite effects on most of the determined parameters; it improved the efficiency of photosynthesis in the cucumber seedlings both at cold stress and at control ambient temperature. In addition, we recorded significant alleviation of the cold stress effect on sugar contents in leaves, which indicated that higher carbon-sink strength was an important factor maintaining higher efficiency of photosynthesis in mycorrhizal cucumber seedlings under cold stress.

Keywords: arbuscular mycorrhizal fungi; carbohydrate; chlorophyll a fluorescence; cold stress; Cucumis sativus L.

Received: May 18, 2017; Accepted: April 23, 2018; Prepublished online: December 5, 2018; Published: January 30, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
MA, J., JANOUŠKOVÁ, M., YE, L., BAI, L.Q., DONG, R.R., YAN, Y., ... HE, C.X. (2019). Role of arbuscular mycorrhiza in alleviating the effect of cold on the photosynthesis of cucumber seedlings. Photosynthetica57(1), 86-95. doi: 10.32615/ps.2019.001.
Download citation

References

  1. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions. - Plant Physiol. 141: 391-396, 2006. Go to original source...
  2. Ashraf M., Harris P.J.C.: Photosynthesis under stressful environ-ments: an overview. - Photosynthetica 51: 163-190, 2013. Go to original source...
  3. Augé R.M., Toler H.D., Saxton A.M.: Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. - Mycorrhiza 25: 13-24, 2015. Go to original source...
  4. Badiani M., Paolacci A.R, D'Annibale A. et al.: Antioxidants and photosynthesis in the leaves of Triticum durum L. seedlings acclimated to low, non-chilling temperature. - J. Plant Physiol. 142: 18-24, 1993. Go to original source...
  5. Bago B., Pfeffer P.E., Abubaker J. et al.: Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. - Plant Physiol. 131: 1496-1507, 2003. Go to original source...
  6. Baker N.R.: Chlorophyll fluorescence: a probe of photosynthesis in vivo. - Annu. Rev. Plant Biol. 59: 89-113, 2008. Go to original source...
  7. Baker N.R., Rosenqvist E.: Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. - J. Exp. Bot. 55: 1607-1621, 2004. Go to original source...
  8. Balouchi H.R.: Screening wheat parents of mapping population for heat and drought tolerance, detection of wheat genetic variation. - Int. J. Biol. Life Sci. 6: 431-441, 2010.
  9. Begcy K., Mariano E.D., Gentile A. et al.: A novel stress-induced sugarcane gene confers tolerance to drought, salt and oxidative stress in transgenic tobacco plants. - PLoS ONE 7: e44697, 2012. Go to original source...
  10. Boldt K., Pörs Y., Haupt B. et al.: Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza. - J. Plant Physiol. 168: 1256-1263, 2011. Go to original source...
  11. Bulgarelli R.G., Marcos F.C.C., Ribeiro R.V. et al.: Mycorrhizae enhance nitrogen fixation and photosynthesis in phosphorus-starved soybean (Glycine max L. Merrill). - Environ. Exp. Bot. 140: 26-33, 2017. Go to original source...
  12. Bunn R., Lekberg Y., Zabinski C.: Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants. - Ecology 90: 1378-1388, 2009. Go to original source...
  13. Chen S., Jin W., Liu A. et al.: Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. - Sci. Hortic.-Amsterdam 160: 222-229, 2013.
  14. de Andrade S.A.L., Domingues A.P., Mazzafera P.: Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. - Chemosphere 134: 141-149, 2015. Go to original source...
  15. Doulis A.G., Debian N., Kingston-Smith A.H. et al.: Differential localization of antioxidants in maize leaves. - Plant Physiol. 114: 1031-1037, 1997. Go to original source...
  16. Drüge U., Schonbeck F.: Effect of vesicular-arbuscular mycorrhizal infection on transpiration, photosynthesis and growth of flax (Linum usitatissimum L.) in relation to cytokinin levels. - J. Plant Physiol. 141: 40-48, 1993. Go to original source...
  17. Farquhar G.D., Sharkey T.D.: Stomatal conductance and photosynthesis. - Annu. Rev. Plant Physio. 33: 317-345, 1982. Go to original source...
  18. Fay P., Mitchell D., Osborne B.: Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus. - New Phytol. 132: 425-433, 1996. Go to original source...
  19. Finlay R.D.: Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. - J. Exp. Bot. 59: 1115-1126, 2008. Go to original source...
  20. Fracheboud Y., Haldimann P., Leipner J. et al.: Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). - J. Exp. Bot. 50: 1533-1540, 1999. Go to original source...
  21. Gupta A.K., Kaur N.: Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. - J. Biosci. 30: 761-776, 2005. Go to original source...
  22. Hajiboland R., Aliasgharzadeh N., Laiegh S.F. et al.: Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. - Plant Soil 331: 313-327, 2010. Go to original source...
  23. Han Y.S.: Food Chemical Experiment Guidance. Pp. 75-77. China Agricultural University Press, Beijing 1996.
  24. Hanway J.J., Heidel H.: Soil analysis methods as used in Iowa state college soil testing laboratory. - Iowa Agriculture 7: 364-374, 1952.
  25. Hetrick B.D., Bloom J.: The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. - Mycologia 76: 953-956, 1984. Go to original source...
  26. Hu L.P., Meng F.Z., Wang S.H. et al.: Changes in carbohydrate levels and their metabolic enzymes in leaves, phloem sap and mesocarp during cucumber (Cucumis sativus L.) fruit development. - Sci. Hortic.-Amsterdam 121: 131-137, 2009. Go to original source...
  27. Jamil M., Lee K.J., Kim J.M. et al.: Salinity reduced growth PS2 photochemistry and chlorophyll content in radish. - Sci. Agr. 64: 111-118, 2007. Go to original source...
  28. Janicka-Russak M., Kabała K., Wdowikowska A. et al.: Response of plasma membrane H+-ATPase to low temperature in cucumber roots. - J. Plant Res. 125: 291-300, 2012. Go to original source...
  29. Kaschuk G., Kuyper T.W., Leffelaar P.A. et al.: Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? - Soil Biol. Biochem. 41: 1233-1244, 2009. Go to original source...
  30. Kachurina O.M., Zhang H., Raun W.R. et al.: Simultaneous determination of soil aluminum, ammonium- and nitrate-nitrogen using 1 M potassium chloride extraction. - Commun. Soil Sci. Plan. 31: 893-90, 2000. Go to original source...
  31. Latef A.A.H.A., He C.: Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. - Acta. Physiol. Plant. 33: 1217-1225, 2011. Go to original source...
  32. Liu A., Chen S., Chang R. et al.: Arbuscular mycorrhizae improve low temperature tolerance in cucumber via alterations in H2O2 accumulation and ATPase activity. - J. Plant Res. 127: 775-785, 2014. Go to original source...
  33. Liu A., Wang B., Hamel C.: Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature. - Mycorrhiza 14: 93-101, 2004. Go to original source...
  34. Liu Z., Bie Z., Huang Y. et al.: Grafting onto Cucurbita moschata rootstock alleviates salt stress in cucumber plants by delaying photoinhibition. - Photosynthetica 50: 152-160, 2012. Go to original source...
  35. Ma J., Janoušková M., Li Y.S. et al.: Impact of arbuscular mycorrhizal fungi (AMF) on cucumber growth and phosphorus uptake under cold stress. - Funct. Plant Biol. 42: 1158-1167, 2015. Go to original source...
  36. Malcová R., Gryndler M.: Amelioration of Pb and Mn toxicity to arbuscular mycorrhizal fungus Glomus intraradices by maize root exudates. - Biol. Plantarum 47: 297-299, 2003.
  37. Martin C.A., Stutz J.C.: Interactive effects of temperature and arbuscular mycorrhizal fungi on growth, P uptake and root respiration of Capsicum annuum L. - Mycorrhiza 14: 241-244, 2004. Go to original source...
  38. Maxwell K., Johnson G.N.: Chlorophyll fluorescence - a practical guide. - J. Exp. Bot. 51: 659-668, 2000. Go to original source...
  39. McGonigle T., Miller M., Evans D. et al.: A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. - New Phytol. 115: 495-501, 1990. Go to original source...
  40. Murata N., Takahashi S., Nishiyama Y. et al.: Photoinhibition of photosystem II under environmental stress. - BBA-Bioenergetics 1767: 414-421, 2007. Go to original source...
  41. Nowak J.: Effects of arbuscular mycorrhizal fungi and organic fertilization on growth, flowering, nutrient uptake, photosynthesis and transpiration of geranium (Pelargonium hortorum L.H. Bailey'Tango Orange'). - Symbiosis 37: 259-266, 2004.
  42. Oliveira G., Peñuelas J.: Effects of winter cold stress on photosynthesis and photochemical efficiency of PSII of the Mediterranean Cistus albidus L. and Quercus ilex L. - Plant Ecol. 175: 179-191, 2005. Go to original source...
  43. Olsen S.R., Cole C., Watanabe F. et al.: Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular 939. Pp. 1-19. United States Department of Agriculture, Washington, DC 1954.
  44. Oquist G., Huner N.: Effects of cold acclimation on the susceptibility of photosynthesis to photoinhibition in Scots pine and in winter and spring cereals: a fluorescence analysis. - Funct. Ecol. 5: 91-100, 1991. Go to original source...
  45. Phillips J.M., Hayman D.S.: Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. - Trans. Brit. Mycol. Soc. 55: 158-160,1970. Go to original source...
  46. Pinior A., Grunewaldt-Stöcker G., von Alten H. et al.: Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring. - Mycorrhiza 15: 596-605, 2005. Go to original source...
  47. Porcel R., Redondo-Gómez S., Mateos-Naranjo E. et al.: Arbuscular mycorrhizal symbiosis ameliorates the optimum quantum yield of photosystem II and reduces non-photochemical quenching in rice plants subjected to salt stress. - J. Plant Physiol. 185: 75-83, 2015. Go to original source...
  48. Ruelland E., Vaultier M.N., Zachowski A. et al.: Cold signalling and cold acclimation in plants. - Adv. Bot. Res. 49: 35-150, 2009. Go to original source...
  49. Ruotsalainen A.L., Kytöviita M.M.: Mycorrhiza does not alter low temperature impact on Gnaphalium norvegicum. - Oecologia 140: 226-233, 2004. Go to original source...
  50. Saltveit M.E.Jr., Morris L.L.: Overview on chilling injury of horticultural crops - In: Wang C.Y. (ed.): Chilling Injury of Horticultural Crops. Pp. 3-15. CRC Press, Boca Raton 1990.
  51. Schöner S., Heinrich Krause G.: Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. - Planta 180: 383-389, 1990. Go to original source...
  52. Schüßler A., Walker C.: The Glomeromycota: a species list with new families and new genera. Pp. 57. Gloucester 2010.
  53. Schüßler A., Schwarzott D., Walker C.: A new fungal phylum, the Glomeromycota: phylogeny and evolution Dedicated to Manfred Kluge (Technische Universität Darmstadt) on the occasion of his retirement. - Mycol. Res. 105: 1413-1421, 2001.
  54. Selosse M.A., Richard F., He X. et al.: Mycorrhizal networks: des liaisons dangereuses? - Trends Ecol. Evol. 21: 621-628, 2006. Go to original source...
  55. Sheng M., Tang M., Chen H. et al.: Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. - Mycorrhiza 18: 287-296, 2008. Go to original source...
  56. Shu S., Yuan L.Y., Guo S.R. et al.: Effects of exogenous spermidine on photosynthesis, xanthophyll cycle and endogenous polyamines in cucumber seedlings exposed to salinity. - Afr. J. Biotechnol. 11: 6064-6074, 2014.
  57. Smith S., Read D.: Mycorrhizal Symbiosis, 3rd Ed. Pp. 30. Academic Press, London 2008.
  58. Solaiman M.Z., Saito M.: Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. - New Phytol. 136: 533-538, 1997. Go to original source...
  59. Stitt M., Hurry V.: A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. - Curr. Opin. Plant Biol. 5: 199-206, 2002. Go to original source...
  60. Su C.F., Wang Y.C., Hsieh T.H. et al.: A novel MYBS3-dependent pathway confers cold tolerance in rice. - Plant Physiol. 153: 145-158, 2010. Go to original source...
  61. Tang Y., Wen X., Lu Q. et al.: Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. - Plant Physiol. 143: 629-638, 2007. Go to original source...
  62. Vaz J., Sharma P.K.: Relationship between xanthophyll cycle and non-photochemical quenching in rice (Oryza sativa L.) plants in response to light stress. - Indian J. Exp. Bot. 49: 60-67, 2011.
  63. Vonshak A., Torzillo G., Masojídek J. et al.: Sub-optimal morning temperature induces photoinhibition in dense outdoor cultures of the alga Monodus subterraneus (Eustigmatophyta). - Plant Cell Environ. 24: 1113-1118, 2001. Go to original source...
  64. Wang B., Funakoshi D., Dalpé Y. et al.: Phosphorus-32 absorption and translocation to host plants by arbuscular mycorrhizal fungi at low root-zone temperature. - Mycorrhiza 12: 93-96, 2002. Go to original source...
  65. Willekens H., Chamnongpol S., Davey M. et al.: Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. - EMBO J. 16: 4806-4816, 1997. Go to original source...
  66. Wright D., Scholes J., Read D.: Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. - Plant Cell Environ. 21: 209-216, 1998. Go to original source...
  67. Wu Q.S., Xia R.X.: Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. - J. Plant Physiol. 163: 417-425, 2006. Go to original source...
  68. Wu Q.S., Zou Y.N.: Beneficial roles of arbuscular mycorrhizas in citrus seedlings at temperature stress. - Sci. Hortic.-Amsterdam 125: 289-293, 2010.
  69. Xin Z., Browse J.: Cold comfort farm: the acclimation of plants to freezing temperatures. - Plant Cell Environ. 23: 893-902, 2000. Go to original source...
  70. Yadav S.K.: Cold stress tolerance mechanisms in plants. A review. - Agron. Sustain. Dev. 30: 515-527, 2010. Go to original source...
  71. Zhang W., Jiang B., Li W. et al.: Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. - Sci. Hortic.-Amsterdam 122: 200-208, 2009.
  72. Zhu X.C., Song F.B., Xu H.W.: Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. - Plant Soil 331: 129-137, 2010a. Go to original source...
  73. Zhu X., Song F., Xu H.: Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. - Mycorrhiza 20: 325-332, 2010b. Go to original source...
  74. Zlatev Z.: Drought-induced changes in chlorophyll fluorescence of young wheat plants. - Biotechnol. Biotec. Eq. 23: 438-441, 2009. Go to original source...