Temporal complementarity between roots and mycorrhizal fungi drives wheat nitrogen use efficiency.
arbuscular mycorrhiza
functional complementarity
nitrogen utilisation efficiency
root traits
wheat
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
received:
31
05
2022
accepted:
26
07
2022
pubmed:
6
8
2022
medline:
12
10
2022
entrez:
5
8
2022
Statut:
ppublish
Résumé
Improving nitrogen (N) use efficiency (NUE) to reduce the application of N fertilisers in a way that benefits the environment and reduces farmers' costs is an ongoing objective for sustainable wheat production. However, whether and how arbuscular mycorrhizal fungi (AMF) affect NUE in wheat is still not well explored. Three independent but complementary experiments were conducted to decipher the contribution of roots and AMF to the N uptake and utilisation efficiency in wheat. We show a temporal complementarity pattern between roots and AMF in shaping NUE of wheat. Pre-anthesis N uptake efficiency mainly depends on root functional traits, but the efficiency to utilise the N taken up during pre-anthesis for producing grains (E
Substances chimiques
Fertilizers
0
Soil
0
Phosphorus
27YLU75U4W
Carbon
7440-44-0
Nitrogen
N762921K75
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1168-1181Informations de copyright
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.
Références
Aranjuelo I, Cabrera-Bosquet L, Araus JL, Nogues S. 2013. Carbon and nitrogen partitioning during the post-anthesis period is conditioned by N fertilisation and sink strength in three cereals. Plant Biology 15: 135-143.
Arduini I, Masoni A, Ercoli L, Mariotti M. 2006. Grain yield, and dry matter and nitrogen accumulation and remobilization in durum wheat as affected by variety and seeding rate. European Journal of Agronomy 25: 309-318.
Averill C, Bhatnagar JM, Dietze MC, Pearse WD, Kivlin SN. 2019. Global imprint of mycorrhizal fungi on whole-plant nutrient economics. Proceedings of the National Academy of Sciences, USA 116: 23163-23168.
Bago B, Pfeffer PE, Shachar-Hill Y. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124: 949-957.
Baresel JP, Zimmermann G, Reents HJ. 2008. Effects of genotype and environment on N uptake and N partition in organically grown winter wheat (Triticum aestivum L.) in Germany. Euphytica 163: 347-354.
Barraclough PB, Lopez-Bellido R, Hawkesford MJ. 2014. Genotypic variation in the uptake, partitioning and remobilisation of nitrogen during grain-filling in wheat. Field Crops Research 156: 242-248.
Benlloch-Gonzalez M, Berger J, Bramley H, Rebetzke G, Palta JA. 2014. The plasticity of the growth and proliferation of wheat root system under elevated CO2. Plant and Soil 374: 963-976.
Bergmann J, Weigelt A, van der Plas F, Laughlin DC, Kuyper TW, Guerrero-Ramirez NR, Valverde-Barrantes OJ, Bruelheide H, Freschet GT, Iversen CM et al. 2020. The fungal collaboration gradient dominates the root economics space in plants. Science Advances 6: eaba3756.
Black KG, Mitchell DT, Osborne BA. 2000. Effect of mycorrhizal-enhanced leaf phosphate status on carbon partitioning, translocation and photosynthesis in cucumber. Plant, Cell & Environment 23: 797-809.
Blum A. 1998. Improving wheat grain filling under stress by stem reserve mobilisation. Euphytica 100: 77-83.
Bogard M, Allard V, Brancourt-Hulmel M, Heumez E, Machet J-M, Jeuffroy M-H, Gate P, Martre P, Le Gouis J. 2010. Deviation from the grain protein concentration-grain yield negative relationship is highly correlated to post-anthesis N uptake in winter wheat. Journal of Experimental Botany 61: 4303-4312.
Bossio DA, Scow KM. 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology 35: 265-278.
Bryla DR, Duniway JM. 1997. Growth, phosphorus uptake, and water relations of safflower and wheat infected with an arbuscular mycorrhizal fungus. New Phytologist 136: 581-590.
Bueno CG, Gerz M, Moora M, Leon D, Gomez-Garcia D, de Leon DG, Font X, Al-Quraishy S, Hozzein WN, Zobel M. 2021. Distribution of plant mycorrhizal traits along an elevational gradient does not fully mirror the latitudinal gradient. Mycorrhiza 31: 149-159.
Chagnon P-L, Bradley RL, Maherali H, Klironomos JN. 2013. A trait-based framework to understand life history of mycorrhizal fungi. Trends in Plant Science 18: 484-491.
Chen YL, Xu ZW, Xu TL, Veresoglou SD, Yang GW, Chen BD. 2017. Nitrogen deposition and precipitation induced phylogenetic clustering of arbuscular mycorrhizal fungal communities. Soil Biology & Biochemistry 115: 233-242.
Dordas C. 2009. Dry matter, nitrogen and phosphorus accumulation, partitioning and remobilization as affected by N and P fertilization and source-sink relations. European Journal of Agronomy 30: 129-139.
Duan HX, Luo CL, Li JY, Wang BZ, Naseer M, Xiong YC. 2021. Improvement of wheat productivity and soil quality by arbuscular mycorrhizal fungi is density- and moisture-dependent. Agronomy for Sustainable Development 41: 3.
Eroglu CG, Cabral C, Ravnskov S, Bak Topbjerg H, Wollenweber B. 2020. Arbuscular mycorrhiza influences carbon-use efficiency and grain yield of wheat grown under pre- and post-anthesis salinity stress. Plant Biology 22: 863-871.
Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Buecking H. 2012. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 109: 2666-2671.
Gaju O, Allard V, Martre P, Le Gouis J, Moreau D, Bogard M, Hubbart S, Foulkes MJ. 2014. Nitrogen partitioning and remobilization in relation to leaf senescence, grain yield and grain nitrogen concentration in wheat cultivars. Field Crops Research 155: 213-223.
Garcia de Leon D, Vahter T, Zobel M, Koppel M, Edesi L, Davison J, Al-Quraishy S, Hozzein WN, Moora M, Oja J et al. 2020. Different wheat cultivars exhibit variable responses to inoculation with arbuscular mycorrhizal fungi from organic and conventional farms. PLoS ONE 15: e0233878.
Giovannetti M, Mosse B. 1980. An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytologist 84: 489-500.
Han YF, Feng JG, Han MG, Zhu B. 2020. Responses of arbuscular mycorrhizal fungi to nitrogen addition: a meta-analysis. Global Change Biology 26: 7229-7241.
Hawkesford MJ. 2014. Reducing the reliance on nitrogen fertilizer for wheat production. Journal of Cereal Science 59: 276-283.
Jakobsen I, Abbott LK, Robson AD. 1992. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytologist 120: 371-380.
Jiang YN, Wang WX, Xie QJ, Liu N, Liu LX, Wang DP, Zhang XW, Yang C, Chen XY, Tang DZ et al. 2017. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356: 1172-1175.
Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J. 2007. In winter wheat (Triticum aestivum L.), post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers. Field Crops Research 102: 22-32.
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882.
Koide RT. 2000. Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytologist 147: 233-235.
Kong D, Wang J, Wu H, Valverde-Barrantes OJ, Wang R, Zeng H, Kardol P, Zhang H, Feng Y. 2019. Nonlinearity of root trait relationships and the root economics spectrum. Nature Communications 10: 2203.
Lee J, Lee S, Young JPW. 2008. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiology Ecology 65: 339-349.
Lehnert H, Serfling A, Enders M, Friedt W, Ordon F. 2017. Genetics of mycorrhizal symbiosis in winter wheat (Triticum aestivum L.). New Phytologist 215: 779-791.
Li HY, Smith FA, Dickson S, Holloway RE, Smith SE. 2008. Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytologist 178: 852-862.
Li HY, Zhu YG, Marschner P, Smith FA, Smith SE. 2005. Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant and Soil 277: 221-232.
Lu RK. 1999. The analysis method of soil agricultural chemistry. Beijing, China: China Agricultural Science and Technology Press.
Lv XK, Han J, Liao YC, Liu Y. 2017. Effect of phosphorus and potassium foliage application post-anthesis on grain filling and hormonal changes of wheat. Field Crops Research 214: 83-93.
Ma ZQ, Guo DL, Xu XL, Lu MZ, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO. 2018. Evolutionary history resolves global organization of root functional traits. Nature 555: 94-97.
Mader P, Kaiser F, Adholeya A, Singh R, Uppal HS, Sharma AK, Srivastava R, Sahai V, Aragno M, Wiemken A et al. 2011. Inoculation of root microorganisms for sustainable wheat-rice and wheat-black gram rotations in India. Soil Biology & Biochemistry 43: 609-619.
Maherali H, Klironomos JN. 2007. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316: 1746-1748.
Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M. 2008. Leaf nitrogen remobilisation for plant development and grain filling. Plant Biology 10: 23-36.
Moll RH, Kamprath EJ, Jackson WA. 1982. Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal 74: 562-564.
Oury FX, Chiron H, Faye A, Gardet O, Giraud A, Heumez E, Rolland B, Rousset M, Trottet M, Charmet G et al. 2010. The prediction of bread wheat quality: joint use of the phenotypic information brought by technological tests and the genetic information brought by HMW and LMW glutenin subunits. Euphytica 171: 87-109.
Palta J, Watt M. 2009. Vigorous crop root systems: form and function for improving the capture of water and nutrients. In: Sadras V, Calderini D, eds. Crop physiology: applications for genetic improvement and agronomy. San Diego, CA, USA: Academic Press, 309-325.
Pan J, Zhu Y, Cao WX. 2007. Modeling plant carbon flow and grain starch accumulation in wheat. Field Crops Research 101: 276-284.
Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ, Keys AJ. 2003. Manipulation of Rubisco: the amount, activity, function and regulation. Journal of Experimental Botany 54: 1321-1333.
Pellegrino E, Opik M, Bonari E, Ercoli L. 2015. Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biology & Biochemistry 84: 210-217.
Plenchette C, Fortin JA, Furlan VJP. 1983. Growth response of several plants species to mycorrhiza in a soil of moderate P fertility. I. Mycorrhizal dependency under field conditions. Plant and Soil 70: 199-209.
Reich PB. 2014. The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102: 275-301.
Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A. 2015. Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytologist 205: 1385-1388.
Rillig MC, Aguilar-Trigueros CA, Camenzind T, Cavagnaro TR, Degrune F, Hohmann P, Lammel DR, Mansour I, Roy J, van der Heijden MGA et al. 2019. Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytologist 222: 1171-1175.
Roch GV, Maharajan T, Ceasar SA, Ignacimuthu S. 2019. The role of Pht1 family transporters in the acquisition and redistribution of phosphorus in plants. Critical Reviews in Plant Sciences 38: 171-198.
Ryan MH, Graham JH. 2018. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytologist 220: 1092-1107.
Sanchez-Bragado R, Molero G, Reynolds MP, Luis AJ. 2014. Relative contribution of shoot and ear photosynthesis to grain filling in wheat under good agronomical conditions assessed by differential organ delta C-13. Journal of Experimental Botany 65: 5401-5413.
Sangwan S, Prasanna R. 2021. Mycorrhizae helper bacteria: unlocking their potential as bioenhancers of plant-arbuscular mycorrhizal fungal associations. Microbial Ecology 84: 1-10.
Sawers RJH, Rosario Ramirez-Flores M, Olalde-Portugal V, Paszkowski U. 2018. The impact of domestication and crop improvement on arbuscular mycorrhizal symbiosis in cereals: insights from genetics and genomics. New Phytologist 220: 1135-1140.
Sheteiwy MS, Ulhassan Z, Qi W, Lu H, AbdElgawad H, Minkina T, Sushkova S, Rajput VD, El-Keblawy A, Josko I et al. 2022. Association of jasmonic acid priming with multiple defense mechanisms in wheat plants under high salt stress. Frontiers in Plant Science 13: 886862.
Sieling K, Kage H. 2021. Apparent fertilizer N recovery and the relationship between grain yield and grain protein concentration of different winter wheat varieties in a long-term field trial. European Journal of Agronomy 124: 126246.
Simmonds NW. 1995. The relation between yield and protein in cereal grain. Journal of the Science of Food and Agriculture 67: 309-315.
Simon L, Lalonde M, Bruns TD. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Applied and Environmental Microbiology 58: 291-295.
Smith AP, Marin-Spiotta E, Balser T. 2015. Successional and seasonal variations in soil and litter microbial community structure and function during tropical postagricultural forest regeneration: a multiyear study. Global Change Biology 21: 3532-3547.
Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn. San Diego, CA, USA: Academic Press.
Tennant D. 1975. A test of a modified line intersection method of measuring root length. Journal of Ecology 63: 995-1001.
Treseder KK. 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164: 347-355.
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J. 2006. A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314: 1298-1301.
Verzeaux J, Hirel B, Dubois F, Lea PJ, Tetu T. 2017. Agricultural practices to improve nitrogen use efficiency through the use of arbuscular mycorrhizae: basic and agronomic aspects. Plant Science 264: 48-56.
Vierheilig HCA, Wyss U, Piche Y. 1998. Ink and vinegar, a simple staining technique for arbuscular mycorrhizal fungi. Applied and Environmental Microbiology 64: 5004-5007.
Weih M, Asplund L, Bergkvist G. 2011. Assessment of nutrient use in annual and perennial crops: a functional concept for analyzing nitrogen use efficiency. Plant and Soil 339: 513-520.
Weih M, Liu H, Colombi T, Keller T, Jack O, Vallenback P, Westerbergh A. 2021. Evidence for magnesium-phosphorus synergism and co-limitation of grain yield in wheat agriculture. Scientific Reports 11: 9012.
Wen ZH, Li HB, Shen Q, Tang XM, Xiong CY, Li HG, Pang JY, Ryan MH, Lambers H, Shen JB. 2019. Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytologist 223: 882-895.
Wu K, Chen D, Tu C, Qiu Y, Burkey KO, Reberg-Horton SC, Peng S, Hu S. 2017. CO2-induced alterations in plant nitrate utilization and root exudation stimulate N2O emissions. Soil Biology and Biochemistry 106: 9-17.
Yang H, Zhang Q, Dai Y, Liu Q, Tang J, Bian X, Chen X. 2015. Effects of arbuscular mycorrhizal fungi on plant growth depend on root system: a meta-analysis. Plant and Soil 389: 361-374.
Zhang L, Zhou J, George TS, Limpens E, Feng G. 2022. Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends in Plant Science 27: 402-411.
Zhang SJ, Lehmann A, Zheng WS, You ZY, Rillig MC. 2019. Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytologist 222: 543-555.
Zhang SJ, Wang L, Ma F, Bloomfield KJ, Yang JX, Atkin OK. 2015. Is resource allocation and grain yield of rice altered by inoculation with arbuscular mycorrhizal fungi? Journal of Plant Ecology 8: 436-448.
Zhang Z, Phillips RP, Zhao W, Yuan Y, Liu Q, Yin H. 2019. Mycelia-derived C contributes more to nitrogen cycling than root-derived C in ectomycorrhizal alpine forests. Functional Ecology 33: 346-359.
Zheng T, Miltner A, Liang C, Nowak KM, Kastner M. 2021. Turnover of gram-negative bacterial biomass-derived carbon through the microbial food web of an agricultural soil. Soil Biology & Biochemistry 152: 108070.
Zhou BW, Serret MD, Pie JB, Shah SS, Li ZJ. 2018. Relative contribution of nitrogen absorption, remobilization, and partitioning to the ear during grain filling in Chinese winter wheat. Frontiers in Plant Science 9: 1351.
Zhu X, Song F, Liu S, Liu F. 2016. Arbuscular mycorrhiza improve growth, nitrogen uptake, and nitrogen use efficiency in wheat grown under elevated CO2. Mycorrhiza 26: 133-140.
Zoerb C, Ludewig U, Hawkesford MJ. 2018. Perspective on wheat yield and quality with reduced nitrogen supply. Trends in Plant Science 23: 1029-1037.
Zou JW, Huang Y, Jiang JY, Zheng XH, Sass RL. 2005. A 3-year field measurement of methane and nitrous oxide emissions from rice paddies in China: effects of water regime, crop residue, and fertilizer application. Global Biogeochemical Cycles 19: GB2021.