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Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress

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Abstract

The purpose of this study was to investigate the effects of arbuscular mycorrhizal (AM) symbiosis on gas exchange, chlorophyll fluorescence, pigment concentration and water status of maize plants in pot culture under high temperature stress. Zea mays L. genotype Zhengdan 958 were cultivated in soil at 26/22°C for 6 weeks, and later subjected to 25, 35 and 40°C for 1 week. The plants inoculated with the AM fungus Glomus etunicatum were compared with the non-inoculated plants. The results showed that high temperature stress decreased the biomass of the maize plants. AM symbiosis markedly enhanced the net photosynthetic rate, stomatal conductance and transpiration rate in the maize leaves. Compared with the non-mycorrhizal plants, mycorrhizal plants had lower intercellular CO2 concentration under 40°C stress. The maximal fluorescence, maximum quantum efficiency of PSII photochemistry and potential photochemical efficiency of mycorrhizal plants were significantly higher than corresponding non-mycorrhizal plants under high temperature stress. AM-inoculated plants had higher concentrations of chlorophyll a, chlorophyll b and carotenoid than non-inoculated plants. Furthermore, AM colonization increased water use efficiency, water holding capacity and relative water content. In conclusion, maize roots inoculated with AM fungus may protect the plants against high temperature stress by improving photosynthesis and water status.

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Abbreviations

AM:

arbuscular mycorrhiza

Ci:

intercellular CO2 concentration

E :

transpiration rate

Fm:

maximal fluorescence

Fo:

primary fluorescence

Fv:

variable fluorescence

Fv/Fm:

maximum quantum efficiency of PSII photochemistry

Fv/Fo:

potential photochemical efficiency

gs :

stomatal conductance

Pn:

net photosynthetic rate

PSII:

photosystem II

RWC:

relative water content

WHC:

water holding capacity

WUE:

water use efficiency

References

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    Article  PubMed  CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381

    Article  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958

    Article  PubMed  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  PubMed  CAS  Google Scholar 

  • Bendavid-Val R, Rabinowitch HD, Katan J, Kapulnik Y (1997) Viability of VA-mycorrhizal fungi following soil solarization and fumigation. Plant Soil 195:185–193

    Article  CAS  Google Scholar 

  • Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in high plants. Annu Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Bowen GD (1987) The biology and physiology of infection and its development. In: Safir GR (ed) Ecophysiology of VA mycorrhizal plants. CRC, Boca Raton, pp 27–70

    Google Scholar 

  • Camejo D, Rodríguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcón JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol 162:281–289

    Article  PubMed  CAS  Google Scholar 

  • Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214

    PubMed  CAS  Google Scholar 

  • Entry JA, Rygiewicz PT, Watrud LS, Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Adv Environ Res 7:123–138

    Article  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  PubMed  CAS  Google Scholar 

  • Gavito ME, Schweiger P, Jakobsen I (2003) P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment. Global Change Biol 9:106–116

    Article  Google Scholar 

  • Gavito ME, Olsson PA, Rouhier H, Medina-Rpnafiel A, Jakobsen I, Bago A, Azcon-Aguilar C (2005) Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi. New Phytol 168:179–188

    Article  PubMed  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Goicoechea N, Antolin MC, Sanchez-Diaz M (1997) Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfafa subjected to drought. Physiol Plant 100:989–997

    Article  CAS  Google Scholar 

  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization woth arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327

    Article  CAS  Google Scholar 

  • Hall AE (2001) Crop responses to environment. CRC Press LLC, Boca Raton

    Google Scholar 

  • Haugen LM, Smith SE (1992) The effect of high temperature and fallow period on infection of mung bean and cashew roots by the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. Plant Soil 145:71–80

    Article  Google Scholar 

  • Hawkes CV, Hartley IP, Ineson P, Fitter AH (2008) Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus. Global Change Biol 14:1181–1190

    Article  Google Scholar 

  • Heinemeyer A, Fitter AH (2004) Impact of temperature on the arbuscular mycorrhizal (AM) symbiosis: growth responses of the host plant and its AM fungal partner. J Exp Bot 55:525–534

    Article  PubMed  CAS  Google Scholar 

  • Heinemeyer A, Ridgway KP, Edwards EJ, Benham DG, Young PW, Fitter AH (2004) Impact of soil warming and shading on colonization and community structure of arbuscular mycorrhizal fungi in roots of a native grassland community. Global Change Biol 10:52–64

    Article  Google Scholar 

  • Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of phothsynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J Exp Bot 57:291–302

    Article  PubMed  CAS  Google Scholar 

  • Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53

    Article  PubMed  Google Scholar 

  • Karim MA, Fracheboud Y, Stamp P (1999) Photosynthetic activity of developing leaves of Zea mays is less affected by heat stress than that of developed leaves. Physiol Plant 105:685–693

    Article  CAS  Google Scholar 

  • Kormanik PP, Bryan WC, Schultz RC (1980) Procedure and equipment for staining large number of plant roots for endomycorrhizal assay. Can J Microbiol 26:536–538

    Article  PubMed  CAS  Google Scholar 

  • Krause G, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytol 181:13–34

    Article  PubMed  CAS  Google Scholar 

  • Martin CA, Stutz JC (2004) Interactive effects of temperature and arbuscular mycorrhizal fungi on growth, P uptake and root respiration of Capsicum annuum L. Mycorrhiza 14:241–244

    Article  PubMed  Google Scholar 

  • Matsubara Y, Hirano I, Sassa D, Koshikawa K (2004) Alleviation of high temperature stress in strawberry plants infected with arbuscular mycorrhizal fungi. Environ Control Biol 42:105–111

    Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569

    PubMed  CAS  Google Scholar 

  • Miransari M, Bahrami HA, Rejali F, Malakouti MJ (2008) Using arbuscular mycorrhiza to alleviate the stress of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1206

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Aroca R (2010) Host response to osmotic stresses: stomatal behaviour and water use efficiency of arbuscular mycorrhizal plants. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, pp 239–256

  • Sawers RJH, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13(2):93–97

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U, Berry JA (1977) Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of the photosynthetic apparatus. Planta 136:233–238

    Article  CAS  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as an non-intrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 49–70

    Google Scholar 

  • Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52:712–722

    Article  PubMed  CAS  Google Scholar 

  • Shrestha YH, Ishii T, Kadoya K (1995) Effect of vesicular-arbuscular mycorrhizal fungi on the growth, photosynthesis, transpiration and the distribution of photosynthates of bearing Satsuma mandarin trees. J Jpn Soc Hort Sci 64:517–525

    Article  CAS  Google Scholar 

  • Sikes BA, Powell JR, Rillig MC (2010) Deciphering the relative contributions of multiple functions within plant-microbe symbioses. Ecology 91:1591–1597

    Article  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Smith SE, Roncadori RW (1986) Responses of three vesicular-arbuscular mycorrhizal fungi at four soil temperatures and their effects on cotton growth. New Phytol 104:89–95

    Article  Google Scholar 

  • Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Wahid A, Gelani AM, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Wu Q, Zou Y, Xia R, Wang M (2007) Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot Stud 48:147–154

    Google Scholar 

  • Yamane Y, Shikanai T, Kashino Y, Koike H, Satoh K (2000) Reduction of QA in the dark: another cause of fluorescence Fo increases by high temperatures in higher plants. Photosynth Res 63:23–34

    Article  PubMed  CAS  Google Scholar 

  • Young A (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant 83:702–708

    Article  CAS  Google Scholar 

  • Zhang XZ (1992) Research methods of crop physiology. Agricultural Press, Beijing

    Google Scholar 

  • Zhang ZA, Zhang MS (2006) Experimental guide for plant physiology. High Education Press, Beijing

    Google Scholar 

  • Zhu X, Song F, Xu H (2010) Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza 20:325–332

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This study was financially supported by the National Nature Science Foundation of China (No. 31000679) and the Knowledge Innovation Program of Chinese Academy of Sciences (KSCX2-YW-N-077).

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Correspondence to Xian-Can Zhu.

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Responsible Editor: Katharina Pawlowski.

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Zhu, XC., Song, FB., Liu, SQ. et al. Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 346, 189–199 (2011). https://doi.org/10.1007/s11104-011-0809-8

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  • DOI: https://doi.org/10.1007/s11104-011-0809-8

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