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
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
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
Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in high plants. Annu Rev Plant Physiol 31:491–543
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
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
Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214
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
Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280
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
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
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol 84:489–500
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
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
Hall AE (2001) Crop responses to environment. CRC Press LLC, Boca Raton
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
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
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
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
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
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
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
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
Krause G, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349
Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytol 181:13–34
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
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
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569
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
Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13:309–317
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
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
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
Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421
Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52:712–722
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
Sikes BA, Powell JR, Rillig MC (2010) Deciphering the relative contributions of multiple functions within plant-microbe symbioses. Ecology 91:1591–1597
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
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
Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387
Wahid A, Gelani AM, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223
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
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
Young A (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant 83:702–708
Zhang XZ (1992) Research methods of crop physiology. Agricultural Press, Beijing
Zhang ZA, Zhang MS (2006) Experimental guide for plant physiology. High Education Press, Beijing
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
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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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