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Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress

Plant and Soil volume 408, pages 385–399 (2016)Cite this article

Abstract

Aims

To evaluate the role of the AM symbiosis on nutrient allocation in Triticum aestivum L. cv. 1110 at different growth stages before and after heat-stress at anthesis.

Methods

Measurements of plant biomass and grain yield at anthesis, grain-filling and maturity; determination of macro- and micronutrient concentrations in aboveground biomass; evaluation of AM fungal structures in roots and assessment of light-use efficiency of plants.

Results

AM increased grain number in wheat under heat-stress, and altered nutrient allocation and tiller nutrient composition. Heat increased number of arbuscules in wheat root, whereas number of vesicles and total colonization were unaffected. Heat increased photosystem II yield and the electron transfer rate, whereas non-photochemical quenching decreased during the first 2 days of heat-stress.

Conclusions

Nutrient allocation and –composition in wheat grown under heat-stress were altered by AM symbiosis, which lowered the K/Ca ratio, whereas it was increased by heat-stress. The increased carbon availability in spikes at this developmental stage, related to the C sink strength of the AM symbiosis and its influence on source-sink relationships in the host-plant, resulted in increased number of grains in heat-stressed AM plants.

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Abbreviations

AMF:

Arbuscular mycorrhizal fungi

AM:

Arbuscular mycorrhiza

C:

carbon

N:

nitrogen

P:

phosphorus

Ca:

calcium

Mg:

magnesium

K:

potassium

B:

boron

Cu:

copper

Zn:

zinc

Fe:

iron

Mn:

manganese

DAS:

days after sowing

SWRC:

soil relative water content

FW:

fresh weight

DW:

dry weight

LOQ:

limit of quantification

PSII:

Photosystem II

ΦPSII:

photosystem II yield

ETR:

electron transfer rate

NPQ:

non-photochemical quenching

PAR:

photosynthetically active radiation.

References

  • Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269. doi:10.1007/s00572-003-0265-2

    Article  PubMed  Google Scholar 

  • Asseng S, Ewert F, Martre P, Rötter RP, Lobell DB, Cammarano D, Kimball BA, Ottman MJ, Wall GW, White JW, Reynolds MP, Alderman PD, Prasad PVV, Aggarwal PK, Anothai J, Basso B, Biernath C, Challinor AJ, De Sanctis G, Doltra J, Fereres E, Garcia-Vila M, Gayler S, Hoogenboom G, Hunt LA, Izaurralde RC, Jabloun M, Jones CD, Kersebaum KC, Koehler AK, Müller C, Naresh Kumar S, Nendel C, O’Leary G, Olesen JE, Palosuo T, Priesack E, Eyshi Rezaei E, Ruane AC, Semenov MA, Shcherbak I, Stöckle C, Stratonovitch P, Streck T, Supit I, Tao F, Thorburn PJ, Waha K, Wang E, Wallach D, Wolf J, Zhao Z, Zhu Y (2014) Rising temperatures reduce global wheat production. Nat Clim Chang 5:143–147. doi:10.1038/nclimate2470

    Article  Google Scholar 

  • Augé MR (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42. doi:10.1007/s005720100097

    Article  Google Scholar 

  • Baon JB, Smith SE, Alston AM (1994) Growth response and phosphorus uptake of rye with long and short root hairs: Interactions with mycorrhizal infection. Plant Soil 167:247–254. doi:10.1007/bf00007951

    CAS  Article  Google Scholar 

  • Bati C, Santilli E, Lombardo L (2015) Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels. Mycorrhiza 25:97–108. doi:10.1007/s00572-014-0589-0

    Article  Google Scholar 

  • Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:895–904. doi:10.1007/s00442-012-2258-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Bleiholder H et al (2001) Growth stages of mono-and dicotyledonous plants BBCH Monograph. Federal Biological Research Centre for Agriculture and Forestry

  • Brooker R, Kikvidze Z, Pugnaire FI, Callaway RM, Choler P, Lortie CJ, Michalet R (2005) The importance of importance. Oikos 109:63–70. doi:10.1111/j.0030-1299.2005.13557.x

    Article  Google Scholar 

  • Brown PH, Shelp BJ (1997) Boron mobility in plants. Plant Soil 193:85–101. doi:10.1023/a:1004211925160

    CAS  Article  Google Scholar 

  • Calderini DF, Reynolds MP, Slafer GA (2006) Source–sink effects on grain weight of bread wheat, durum wheat, and triticale at different locations. Aust J Agric Res 57:227–233. doi:10.1071/AR05107

    Article  Google Scholar 

  • Chapman HD, Pratt PF (1961) Methods of analysis for soils, plants, and waters. University of California, Division of Agricultural Sciences, [Riverside]

  • Chen X-H, Zhao B (2009) Arbuscular mycorrhizal fungi mediated uptake of nutrient elements by Chinese milk vetch (Astragalus sinicus L.) grown in lanthanum spiked soil. Biol Fertil Soils 45:675–678. doi:10.1007/s00374-009-0379-6

    CAS  Article  Google Scholar 

  • Daei G, Ardekani MR, Rejali F, Teimuri S, Miransari M (2009) Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol 166:617–625. doi:10.1016/j.jplph.2008.09.013

    CAS  Article  PubMed  Google Scholar 

  • Daft MJ, Chilvers MT, Nicolson TH (1980) Mycorrhizas of the liliflorae I. morphogenesis of Endymion non-scriptus (L.) Garcke and its mycorrhizas in nature. New Phytol 85:181–189. doi:10.1111/j.1469-8137.1980.tb04459.x

    Article  Google Scholar 

  • FAO (2014) FAOSTAT. Food and agriculture organization of the United Nations

  • Farooq M, Bramley H, Palta JA, Siddique KHM (2011) Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci 30:491–507. doi:10.1080/07352689.2011.615687

    Article  Google Scholar 

  • Fay P, Mitchell DT, Osborne BA (1996) Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus. New Phytol 132:425–433. doi:10.1111/j.1469-8137.1996.tb01862.x

    CAS  Article  PubMed  Google Scholar 

  • Ferris RE, Ellis RH, Wheeler TR, Hadley P (1998) Effect of high temperature stress at anthesis on grain yield and biomass of field-grown crops of wheat. Ann Bot 82:631–639

    Article  Google Scholar 

  • Fitter A, Heinemeyer A, Staddon PL (2000) The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytol 147:179–187

    CAS  Article  Google Scholar 

  • Gavito ME, Olsson PA, Rouhier H, Medina-Penafiel 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. doi:10.1111/j.1469-8137.2005.01481.x

    CAS  Article  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x

    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. Glob Chang Biol 14:1181–1190. doi:10.1111/j.1365-2486.2007.01535.x

    Article  Google Scholar 

  • IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part a: global and sectoral aspects. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, and New York

    Google Scholar 

  • Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334. doi:10.1046/j.0028-646X.2001.00316.x

    CAS  Article  Google Scholar 

  • Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244. doi:10.1016/j.soilbio.2009.03.005

    CAS  Article  Google Scholar 

  • Katz RW, Brown BG (1992) Extreme events in a changing climate: Variability is more important than averages. Clim Chang 21:289–302. doi:10.1007/bf00139728

    Article  Google Scholar 

  • Kaya C, Higgs D, Kirnak H, Tas I (2003) Mycorrhizal colonisation improves fruit yield and water use efficiency in watermelon (Citrullus lanatus Thunb.) grown under well-watered and water-stressed conditions. Plant Soil 253:287–292. doi:10.1023/a:1024843419670

    CAS  Article  Google Scholar 

  • Kinsel H (1983) Pflanzenökologie und Mineralstoffwechsel. Kinsel, 534 S. In: Kinsel H (ed). Ulmer Verlag, Stuttgart

  • Kirby EJM (1988) Analysis of leaf, stem and ear growth in wheat from terminal spikelet stage to anthesis. Field Crop Res 18:127–140. doi:10.1016/0378-4290(88)90004-4

    Article  Google Scholar 

  • Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops – A meta-analysis. Soil Biol Biochem 81:147–158. doi:10.1016/j.soilbio.2014.11.013

    CAS  Article  Google Scholar 

  • Liu A, Hamel C, Hamilton IR, Ma LB, Smith LD (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336. doi:10.1007/s005720050277

    CAS  Article  Google Scholar 

  • Lobell DB, Tebaldi C (2014) Getting caught with our plants down: the risks of a global crop yield slowdown from climate trends in the next two decades. Environ Res Lett 9:074003. doi:10.1088/1748-9326/9/7/074003

    Article  Google Scholar 

  • Lobell DB, Sibley A, Ivan Ortiz-Monasterio J (2012) Extreme heat effects on wheat senescence in India. Nat Clim Chang 2:186–189. doi:10.1038/nclimate1356

    Article  Google Scholar 

  • Massacci A, Nabiev SM, Pietrosanti L, Nematov SK, Chernikova TN, Thor K, Leipner J (2008) Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiol Biochem 46:189–195. doi:10.1016/j.plaphy.2007.10.006

    CAS  Article  PubMed  Google Scholar 

  • Maya MA, Matsubara Y (2013) Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza 23:381–390. doi:10.1007/s00572-013-0477-z

    CAS  Article  PubMed  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501. doi:10.1111/j.1469-8137.1990.tb00476.x

    Article  Google Scholar 

  • Miller RO (1998) Microwave digestion of plant tissue in a closed vessel. Handbook and reference methods for plant analysis 69–74

  • 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. doi:10.1016/j.soilbio.2007.11.014

    CAS  Article  Google Scholar 

  • Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364. doi:10.1111/j.1469-8137.2004.01169.x

    Article  Google Scholar 

  • Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54:539–547

    CAS  Article  PubMed  Google Scholar 

  • Porter JR, Gawith M (1999) Temperatures and the growth and development of wheat: a review. Eur J Agron 10:23–36

    Article  Google Scholar 

  • Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124. doi:10.1007/bf00202343

    CAS  Article  Google Scholar 

  • Prasad PVV, Staggenborg SA, Ristic Z (2008) Impacts of drought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants. In: Ahuja LR, Reddy VR, Saseendran SA, Yu Q (eds) Response of crops to limited water: understanding and modeling water stress effects on plant growth processes. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison

    Google Scholar 

  • R Core Team (2015) A language and environment for statistical computing. Vienna, Austria. 2014

  • Ravnskov S, Jakobsen I (1995) Functional compatibility in Arbuscular Mycorrhizas measured as hyphal P transport to the plant. New Phytol 129:611–618. doi:10.1111/j.1469-8137.1995.tb03029.x

    Article  Google Scholar 

  • Ravnskov S, Larsen J (2016) Functional compatibility in cucumber mycorrhizas in terms of plant growth performance and foliar nutrient composition. Plant Biol. doi:10.1111/plb.12465

    PubMed  Google Scholar 

  • Rodriguez D, Goudriaan J (1995) Effects of phosphorus and drought stresses on dry matter and phosphorus allocation in wheat. J Plant Nutr 18:2501–2517. doi:10.1080/01904169509365080

    CAS  Article  Google Scholar 

  • Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916. doi:10.1104/pp.15.01935

    CAS  Article  PubMed  Google Scholar 

  • Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250:225–239. doi:10.1023/a:1022839930134

    CAS  Article  Google Scholar 

  • Schapendonk AHCM, Xu HY, Van Der Putten PEL, Spiertz JHJ (2007) Heat-shock effects on photosynthesis and sink-source dynamics in wheat (Triticum aestivum L.). NJAS - Wagening J Life Sci 55:37–54. doi:10.1016/S1573-5214(07)80003-0

    Article  Google Scholar 

  • Slafer GA, Andrade FH (1993) Physiological attributes related to the generation of grain yield in bread wheat cultivars released at different eras. Field Crop Res 31:351–367. doi:10.1016/0378-4290(93)90073-V

    Article  Google Scholar 

  • Slafer GA, Savin R (1994) Source-sink relationships and grain mass at different positions whitin the spike in wheat. Field Crop Res 37:39–49

    Article  Google Scholar 

  • Staddon PL, Gregersen R, Jakobsen I (2004) The response of two Glomus mycorrhizal fungi and a fine endophyte to elevated atmospheric CO2, soil warming and drought. Glob Chang Biol 10:1909–1921. doi:10.1111/j.1365-2486.2004.00861.x

    Article  Google Scholar 

  • Tewolde H, Fernandez CJ, Erickson CA (2006) Wheat cultivars adapted to post-heading high temperature stress. J Agron Crop Sci 192:111–120. doi:10.1111/j.1439-037X.2006.00189.x

    Article  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vignjevic M, Wang X, Olesen JE, Wollenweber B (2015) Traits in spring wheat cultivars associated with yield loss caused by a heat stress episode after anthesis. J Agron Crop Sci 201:32–48. doi:10.1111/jac.12085

    CAS  Article  Google Scholar 

  • Walter J, Kreyling J, Singh BK, Jentsch A (2016) Effects of extreme weather events and legume presence on mycorrhization of Plantago lanceolata and Holcus lanatus in the field. Plant Biol 18:262–270. doi:10.1111/plb.12379

    CAS  Article  PubMed  Google Scholar 

  • Wang M, Christie P, Xiao Z, Qin C, Wang P, Liu J, Xie Y, Xia R (2008) Arbuscular mycorrhizal enhancement of iron concentration by Poncirus trifoliata L. Raf and citrus reticulata Blanco grown on sand medium under different pH. Biol Fertil Soils 45:65–72. doi:10.1007/s00374-008-0290-6

    CAS  Article  Google Scholar 

  • Wardlaw I, Wrigley C (1994) Heat tolerance in temperate cereals: an overview. Funct Plant Biol 21:695–703. doi:10.1071/PP9940695

    Google Scholar 

  • Wollenweber B, Porter J, Schellberg J (2003) Lack of interaction between extreme high-temperature events at vegetative and reproductive growth stages in wheat. J Agron Crop Sci 189:142–150

    Article  Google Scholar 

  • Zahedi M, Jenner CF (2003) Analysis of effects in wheat of high temperature on grain filling attributes estimated from mathematical models of grain filling. J Agric Sci 141:203–212

    Article  Google Scholar 

  • Zhang X, Cai J, Wollenweber B, Liu F, Dai T, Cao W, Jiang D (2013) Multiple heat and drought events affect grain yield and accumulations of high molecular weight glutenin subunits and glutenin macropolymers in wheat. J Cereal Sci 57:134–140. doi:10.1016/j.jcs.2012.10.010

    CAS  Article  Google Scholar 

  • Zhang BB, Chang SX, Anyia AO (2016) Mycorrhizal inoculation and nitrogen fertilization affect the physiology and growth of spring wheat under two contrasting water regimes. Plant Soil 398:47–57. doi:10.1007/s11104-015-2635-x

    CAS  Article  Google Scholar 

  • Zhou Q, Ravnskov S, Jiang D, Wollenweber B (2014) Changes in carbon and nitrogen allocation, growth and grain yield induced by arbuscular mycorrhizal fungi in wheat (Triticum aestivum L.) subjected to a period of water deficit. Plant Growth Regul 75:751–760. doi:10.1007/s10725-014-9977-x

    Article  Google Scholar 

  • Zhu X-C, Song F-B, Liu S-Q, Liu T-D (2011) Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 346:189–199. doi:10.1007/s11104-011-0809-8

    CAS  Article  Google Scholar 

  • Zhu XC, Song FB, Liu SQ, Liu FL (2016) Arbuscular mycorrhiza improve growth, nitrogen uptake, and nitrogen use efficiency in wheat grown under elevated CO2. Mycorrhiza 26:133–140. doi:10.1007/s00572-015-0654-3

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

The authors declare no conflict of interest. This work is mainly financed by the Department of Agroecology of Aarhus University but partially financed by Frands Christian Frantsens Fonden, that contributed to C.C’s stay at Maritsa Vegetable Crops Research Institute in Bulgaria, to perform the nutrient analysis. We would like to thank Sasha Manolova and Evdokia Kazakova for the assistance and guidance with nutrient analyses. We thank Betina Hansen, for the assistance in the semi-field; Steen Meier for the climate chamber assistance and Anne-Pia Larsen for the guidance in the microscopic observations and AMF analyses. Finally, we wish to acknowledge the reviewers and the section editor for the insightful and pertinent comments to this manuscript.

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Authors and Affiliations

  1. Department of Agroecology, Aarhus University, Forsøgsvej 1, DK-4200, Slagelse, Denmark

    Carmina Cabral, Sabine Ravnskov & Bernd Wollenweber

  2. Maritsa Vegetable Crops Research Institute, 32 Brezovsko shosse Str, Plovdiv, 4003, Bulgaria

    Ivanka Tringovska

Authors
  1. Carmina Cabral
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  2. Sabine Ravnskov
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  3. Ivanka Tringovska
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  4. Bernd Wollenweber
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Corresponding author

Correspondence to Sabine Ravnskov.

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Responsible Editor: Thom W. Kuyper.

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Supplementary Fig. 1
figure 5

Daily temperature averages at the outdoor semi-field conditions at the experimental site. Represented are 24 h averages of the temperature (GIF 57 kb)

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Supplementary Fig. 2
figure 6

Total colonization/ root length (m) assessed in (Triticum aestivum L. cv 1110) roots inoculated with arbuscular mycorrhizal fungi (A+) and subjected to heat-stress (H+) or not (H-), and harvested at 46 (1st harvest, Z65), 53 (2nd harvest, Z69) and 121 (3rd harvest, Z89) days after sowing. Values are means (n = 7). Z: growth stage at harvest (Bleiholder et al. 2001) (GIF 29 kb)

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High Resolution Image (TIF 17199 kb)

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Supplementary Table 1

Summary of the effect of soil temperature on arbuscular mycorrhizal fungi growth. Please note that the original nomenclature from the references cited was used in this table. (DOCX 19 kb)

Supplementary Table 2

Macro- and micronutrient concentrations assessed in the tillers of wheat plants (Triticum aestivum L. cv 1110) inoculated with arbuscular mycorrhizal fungi (A+) or not (A-) and harvested at 46 days after sowing (1st harvest, Z65). (DOCX 14 kb)

Supplementary Table 3

Developmental traits assessed in wheat plants (Triticum aestivum L. cv 1110) inoculated with arbuscular mycorrhizal fungi (A+) or not (A-), subjected to heat-stress (H+) or not (H-), and harvested at 46 (1st harvest, Z65), 53 (2nd harvest, Z69) and 121 (3rd harvest, Z89) days after sowing. (DOCX 15 kb)

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Cabral, C., Ravnskov, S., Tringovska, I. et al. Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress. Plant Soil 408, 385–399 (2016). https://doi.org/10.1007/s11104-016-2942-x

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Keywords

  • Arbuscular mycorrhiza
  • Grain number
  • Nutrient allocation
  • Light-use efficiency