Abstract
The effect of arbuscular mycorrhizal (AM) fungus, Glomus etunicatum, on growth, water status, chlorophyll concentration and photosynthesis in maize (Zea mays L.) plants was investigated in pot culture under low temperature stress. The maize plants were placed in a sand and soil mixture at 25°C for 7 weeks, and then subjected to 5°C, 15°C and 25°C for 1 week. Low temperature stress decreased AM root colonization. AM symbiosis stimulated plant growth and had higher root dry weight at all temperature treatments. Mycorrhizal plants had better water status than corresponding non-mycorrhizal plants, and significant differences were found in water conservation (WC) and water use efficiency (WUE) regardless of temperature treatments. AM colonization increased the concentrations of chlorophyll a, chlorophyll b and chlorophyll a + b. The maximal fluorescence (Fm), maximum quantum efficiency of PSII primary photochemistry (Fv/Fm) and potential photochemical efficiency (Fv/Fo) were higher, but primary fluorescence (Fo) was lower in AM plants compared with non-AM plants. AM inoculation notably increased net photosynthetic rate (Pn) and transpiration rate (E) of maize plants. Mycorrhizal plants had higher stomatal conductance (gs) than non-mycorrhizal plants with significant difference only at 5°C. Intercellular CO2 concentration (Ci) was lower in mycorrhizal than that in non-mycorrhizal plants, especially under low temperature stress. The results indicated that AM symbiosis protect maize plants against low temperature stress through improving the water status and photosynthetic capacity.
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Abbreviations
- AM:
-
arbuscular mycorrhiza
- Ci:
-
intercellular CO2 concentration
- E :
-
transpiration rate
- Fm:
-
maximal fluorescence
- Fo:
-
primary fluorescence
- Fv/Fm:
-
maximum quantum efficiency of PSII primary photochemistry
- Fv/Fo:
-
potential photochemical efficiency
- gs :
-
stomatal conductance
- Pn:
-
net photosynthetic rate
- PSII:
-
photosystem II
- RWC:
-
relative water content
- WC:
-
water conservation
- WSD:
-
water saturation deficit
- WUE:
-
water use efficiency
References
Anderson CP, Sucoff EI, Dixon RK (1987) The influence of low soil temperature on the growth of vesicular-arbuscular mycorrhizal Fraxinus pennsylvanica. Can J For Res 17:951–956
Aroca R, Vernieri P, Irigoyen JJ, Sancher-Diaz M, Tognoni F, Pardosso A (2003) Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Sci 165:671–679
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Augé RM, Stodola JW (1990) An apparent increase in symplastic water contributes to greater turgor in mycorrhizal roots of droughted Rosa plants. New Phytol 115:285–295
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958
Bai XF, Han H, Zhou FY, Yang SJ, Liu BC, Lei ZY, Jin Z (2008) Analysis on Dynamic change of relative water content and needle water conservation of Pinus sylvestris var. mongolica on sandy land. Prot For Sci Technol 3:51–54
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Charest C, Dalpé Y, Brown A (1993) The effect of vesicular-arbuscular mycorrhizae and chilling on two hybrids of Zea mays L. Mycorrhiza 4:89–92
Druge U, Schonbeck F (1993) 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
EI-Tohamy W, Schnitzler WH, EI-Behairy U, EI-Beltagy MS (1999) Effect of VA mycorrhiza on improving drought and chilling tolerance of bean plants (Phaseolus vulgaris). J Appl Bot 73:178–183
Faber BA, Zasoski RJ, Munns DN, Shackel K (1991) A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. Can J Bot 69:87–94
Farooq M, Aziz T, Wahid A, Lee DJ, Siddique KHM (2009) Chilling tolerance in maize: agronomic and physiological approaches. Crop Pasture Sci 60:501–516
Fracheboud Y, Haldimann P, Leipner J, Stamp P (1999) Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). J Exp Bot 50:1533–1540
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
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol 84:489–500
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
Hayman S (1974) Plant growth responses to vesicular-arbuscular mycorrhiza. IV. Effect of light and temperature. New Phytol 73:71–80
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 396:525–534
Hetrick BAD, Bloom J (1984) The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. Mycologia 76:953–956
Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rate of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244
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 GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349
Liu A, Wang B, Hamel C (2004) Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature. Mycorrhiza 14:93–101
Martin P (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence- a practical guide. J Exp Bot 51:659–668
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
Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019–1027
Nelsen CE, Safir GR (1982) The water relations of well-watered, mycorrhizal and non-mycorrhizal onion plants. J Am Soc Hort Sci 107:271–274
Paradis R, Dalpé Y, Charest C (1995) The combined effect of arbuscular mycorrhizas and short-term cold exposure on wheat. New Phytol 129:637–642
Sánchez-Díaz M, Pardo M, Antolin M, Peña J, Aguirreolea J (1990) Effect of water stress on photosynthetic activity in the Medicago-Rhizobium-Glomus symbiosis. Plant Sci 71:215–221
Sawers RJH, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13(2):93–97
Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421
Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
Volkmar KM, Woodbury W (1989) Effects of soil temperatures and depth on colonization and root and shoot growth of barley inoculated with vesicular-arbuscular mycorrhizae indigenous to Canadian prairie soil. Can J Bot 67:1702–1707
Wang B, Funakoshi DM, Dalpé Y, Hamel C (2002) 32P absorption and translocation to host plants by AM fungi at low root zone temperature. Mycorrhiza 12:93–96
Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425
Zhang ZA, Zhang MS (2006) Experimental guide for plant physiology. High education, Beijing
Zhang F, Hamel C, Kianmehr H, Smith DL (1995) Root-zone temperature and soybean [Glycine max (L.) Merr.] vesicular-arbuscular mycorrhizae: development and interactions with the nitrogen fixing symbiosis. Environ Exp Bot 35:287–298
Acknowledgements
This study was financially in part supported by the National Basic Research Program of the People’s Republic of China (2009CB118601). We thank Dr. Xiao-Bin Liu for his critical reading of the manuscript.
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Zhu, XC., Song, FB. & Xu, HW. Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331, 129–137 (2010). https://doi.org/10.1007/s11104-009-0239-z
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DOI: https://doi.org/10.1007/s11104-009-0239-z