Arbuscular mycorrhizae reduce the response of important plant functional traits to drought and salinity. A meta-analysis study
Florencia Gobbo A , María José Corriale B C , Ayelén Gázquez D , César Daniel Bordenave D , David Bilenca A C and Ana Menéndez
A C *
+ Author Affiliations
- Author Affiliations
A Departamento de Biodiversidad y Biología Experimental, Facultad de ciencias Exactas y Naturales, Universidad de Buenos Aires, Piso 4° Pabellón II Ciudad Universitaria, Buenos Aires 1428, Argentina.
B Departamento de Ecología, Genética y Evolución, Piso 4° Pabellón II Ciudad Universitaria, Buenos Aires 1428, Argentina.
C Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Piso 4° Pabellón II Ciudad Universitaria, Buenos Aires 1428, Argentina.
D Instituto ‘Cavanilles’ de Biodiversidad y Biología Evolutiva (ICBiBE), Fac. CC. Biológicas, Universitat de València, Burjassot, Valencia 46100, Spain.
Functional Plant Biology 50(5) 407-415 https://doi.org/10.1071/FP22242
Submitted: 11 June 2022 Accepted: 6 March 2023 Published: 24 March 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
We aimed at exploring the plant functional traits whose responses to drought or salinity are altered by the presence of arbuscular mycorrhiza (AM). We performed a meta-analysis across 114 articles spanning 110 plant species or cultivars. We quantified the size effect of AM symbiosis on the stress response of several functional traits, using linear mixed model analysis (LMM). Correlation analysis between functional traits and total biomass responses to stresses were also performed through LMM. The literature search and further selection yielded seven functional traits, extracted from 114 laboratory studies, including 888 observations and 110 plant species/cultivars. Evidence for significant effects of predictor variables (type of stress, AM symbiosis and/or their interaction) on functional trait response were found for leaf area ratio (LAR), root mass fraction (RMF) and root–shoot (R:S) ratio. Our results provided evidence to accept the hypothesis that AM fungal inoculation may reduce the stress response of these plant functional traits by decreasing its magnitude. We also found a weak correlation between stress responses of these traits and total biomass variation. Although our literature search and data collection were intensive and our results robust, the scope of our conclusions is limited by the agronomical bias of plant species targeted by the meta-analysis. Further knowledge on non-cultivable plant species and better understanding of the mechanisms ruling resources allocation in plants would allow more generalised conclusions.
Keywords: arbuscular mycorrhizas, carbon allocation, drought stress, linear mixed-effects models, meta-analysis, plant response, salinity stress.
References
Al-Karaki GN, Al-Raddad A (1997) Effects of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Mycorrhiza 7, 83–88.| Effects of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance.Crossref | GoogleScholarGoogle Scholar |
Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Canadian Journal of Soil Science 84, 373–381.
| Arbuscular mycorrhizae and soil/plant water relations.Crossref | GoogleScholarGoogle Scholar |
Augé RM, Toler HD, Saxton AM (2014) Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Frontiers in Plant Science 5, 562
| Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Frontiers in Plant Science 10, 1068
| Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Burnham KP, Anderson DR (2002) ‘Model selection and inference: a practical information-theoretic approach.’ 2nd edn. (Springer-Verlag: New York, NY, USA)
Chandrasekaran M, Boughattas S, Hu S, Oh S-H, Sa T (2014) A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza 24, 611–625.
| A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress.Crossref | GoogleScholarGoogle Scholar |
Chandrasekaran M, Kim K, Krishnamoorthy R, Walitang D, Sundaram S, Joe MM, Selvakumar G, Hu S, Oh S-H, Sa T (2016) Mycorrhizal symbiotic efficiency on C3 and C4 plants under salinity stress – a meta-analysis. Frontiers in Microbiology 7, 1246
| Mycorrhizal symbiotic efficiency on C3 and C4 plants under salinity stress – a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Chaudhary A, Burivalova Z, Koh LP, Hellweg S (2016) Impact of forest management on species richness: global meta-analysis and economic trade-offs. Scientific Reports 6, 23954
| Impact of forest management on species richness: global meta-analysis and economic trade-offs.Crossref | GoogleScholarGoogle Scholar |
Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi – from ecology to application. Frontiers in Plant Science 9, 1270
| Beneficial services of arbuscular mycorrhizal fungi – from ecology to application.Crossref | GoogleScholarGoogle Scholar |
Cheplick GP (1997) Effects of endophytic fungi on the phenotypic plasticity of Lolium Perenne (Poaceae). American Journal of Botany 84, 34–40.
| Effects of endophytic fungi on the phenotypic plasticity of Lolium Perenne (Poaceae).Crossref | GoogleScholarGoogle Scholar |
Delavaux CS, Smith-Ramesh LM, Kuebbing SE (2017) Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98, 2111–2119.
| Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils.Crossref | GoogleScholarGoogle Scholar |
Echeverria M, Scambato AA, Sannazzaro AI, Maiale S, Ruiz OA, Menéndez AB (2008) Phenotypic plasticity with respect to salt stress response by Lotus glaber: the role of its AM fungal and rhizobial symbionts. Mycorrhiza 18, 317–329.
| Phenotypic plasticity with respect to salt stress response by Lotus glaber: the role of its AM fungal and rhizobial symbionts.Crossref | GoogleScholarGoogle Scholar |
Eissenstat DM (1997) Trade-offs in root form and function. In ‘Ecology in agriculture’. (Ed. LE Jackson) pp. 173–199. (Academic Press: San Diego, CA, USA)
Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Frontiers in Plant Science 10, 470
| Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges.Crossref | GoogleScholarGoogle Scholar |
Eziz A, Yan Z, Tian D, Han W, Tang Z, Fang J (2017) Drought effect on plant biomass allocation: a meta-analysis. Ecology and Evolution 7, 11002–11010.
| Drought effect on plant biomass allocation: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Franco JA, Bañón S, Vicente MJ, Miralles J, Martínez-Sánchez JJ (2011) Root development in horticultural plants grown under abiotic stress conditions – a review. The Journal of Horticultural Science and Biotechnology 86, 543–556.
| Root development in horticultural plants grown under abiotic stress conditions – a review.Crossref | GoogleScholarGoogle Scholar |
Freschet GT, Cornwell WK, Wardle DA, Elumeeva TG, Liu W, Jackson BG, Onipchenko VG, Soudzilovskaia NA, Tao J, Cornelissen JHC (2013) Linking litter decomposition of above- and below-ground organs to plant–soil feedbacks worldwide. Journal of Ecology 101, 943–952.
| Linking litter decomposition of above- and below-ground organs to plant–soil feedbacks worldwide.Crossref | GoogleScholarGoogle Scholar |
Freschet GT, Swart EM, Cornelissen JHC (2015) Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytologist 206, 1247–1260.
| Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction.Crossref | GoogleScholarGoogle Scholar |
Freschet GT, Violle C, Bourget MY, Scherer-Lorenzen M, Fort F (2018) Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress. New Phytologist 219, 1338–1352.
| Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress.Crossref | GoogleScholarGoogle Scholar |
Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
| Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar |
Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. Journal of Experimental Botany 66, 3339–3352.
| Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity.Crossref | GoogleScholarGoogle Scholar |
He Z, Xiong J, Kent AD, Deng Y, Xue K, Wang G, Wu L, Van Nostrand JD, Zhou J (2014) Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem. The ISME Journal 8, 714–726.
| Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem.Crossref | GoogleScholarGoogle Scholar |
Heuer B (2005). Chapter 40: photosynthetic carbon metabolism of crops under salt stress. In ‘Handbook of photosynthesis’. 2nd edn. (Ed. M Pessarakli) pp. 1–14. (Taylor and Francis Group, LLC: Boca Raton, FL)
Hill JO, Simpson RJ, Moore AD, Chapman DF (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant and Soil 286, 7–19.
| Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition.Crossref | GoogleScholarGoogle Scholar |
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13, 394–407.
| A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Hu Y, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. Journal of Plant Nutrition and Soil Science 168, 541–549.
| Drought and salinity: a comparison of their effects on mineral nutrition of plants.Crossref | GoogleScholarGoogle Scholar |
IPCC (2021) Climate change 2021: the physical science basis. Working group I contribution to the IPCC sixth assessment report. IPCC. Available at https://www.ipcc.ch/report/ar6/wg1/
Jayne B, Quigley M (2014) Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza 24, 109–119.
| Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Kadian N, Yadav K, Badda N, Aggarwal A (2013) AM fungi ameliorates growth, yield and nutrient uptake in Cicer arietinum L. under salt stress. Russian Agricultural Sciences 39, 321–329.
| AM fungi ameliorates growth, yield and nutrient uptake in Cicer arietinum L. under salt stress.Crossref | GoogleScholarGoogle Scholar |
Kapoor R, Singh N (2017) Arbuscular mycorrhiza and reactive oxygen species. In ‘Arbuscular mycorrhizas and stress tolerance of plants’. (Ed. QS Wu) pp. 225–243. (Springer: Singapore) https://doi.org/10.1007/978-981-10-4115-0_10
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2019) Estimated marginal means, aka least-squares means R package version 1.4.2. Available at https://cran.r-project.org/package=lsmeans
Marcelis LFM, Heuvelink E, Goudriaan J (1998) Modelling biomass production and yield of horticultural crops: a review. Scientia Horticulturae 74, 83–111.
| Modelling biomass production and yield of horticultural crops: a review.Crossref | GoogleScholarGoogle Scholar |
Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London, UK)
Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant and Soil 159, 89–102.
| Nutrient uptake in mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar |
Martı́nez-Ballesta MC, Martı́nez V, Carvajal M (2004) Osmotic adjustment, water relations and gas exchange in pepper plants grown under NaCl or KCl. Environmental and Experimental Botany 52, 161–174.
| Osmotic adjustment, water relations and gas exchange in pepper plants grown under NaCl or KCl.Crossref | GoogleScholarGoogle Scholar |
Matesanz S, Rubio Teso ML, García-Fernández A, Escudero A (2017) Habitat fragmentation differentially affects genetic variation, phenotypic plasticity and survival in populations of a Gypsum endemic. Frontiers in Plant Science 8, 843
| Habitat fragmentation differentially affects genetic variation, phenotypic plasticity and survival in populations of a Gypsum endemic.Crossref | GoogleScholarGoogle Scholar |
Miranda D, Fischer G, Ulrichs C (2011) The influence of arbuscular mycorrhizal colonization on the growth parameters of cape gooseberry (Physalis peruviana L.) plants grown in a saline soil. Journal in Soil Science and Plant Nutrition 11, 18–30.
| The influence of arbuscular mycorrhizal colonization on the growth parameters of cape gooseberry (Physalis peruviana L.) plants grown in a saline soil.Crossref | GoogleScholarGoogle Scholar |
Molina-Montenegro MA, Naya DE (2012) Latitudinal patterns in phenotypic plasticity and fitness-related traits: assessing the climatic variability hypothesis (CVH) with an invasive plant species. PLoS ONE 7, e47620
| Latitudinal patterns in phenotypic plasticity and fitness-related traits: assessing the climatic variability hypothesis (CVH) with an invasive plant species.Crossref | GoogleScholarGoogle Scholar |
Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
| Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar |
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytologistogist 167, 645–663.
| Genes and salt tolerance: bringing them together.Crossref | GoogleScholarGoogle Scholar |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
| Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar |
Neumann PM, Azaizeh H, Leon D (1994) Hardening of root cell walls: a growth inhibitory response to salinity stress. Plant, Cell & Environment 17, 303–309.
| Hardening of root cell walls: a growth inhibitory response to salinity stress.Crossref | GoogleScholarGoogle Scholar |
Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker MR, Löhmus K, Majdi H, Metcalfe D, Olsthoorn AFM, Pronk A, Vanguelova E, Weih M, Brunner I (2007) Specific root length as an indicator of environmental change. Plant Biosystems –An International Journal Dealing with all Aspects of Plant Biology 141, 426–442.
| Specific root length as an indicator of environmental change.Crossref | GoogleScholarGoogle Scholar |
Pinheiro J, Bates D, DebRoy S, Sarkar D, Heisterkamp S, Van Willigen B (2016) Package ‘nlme’ [Computer software]. Available at https://cranr-projectorg/web/packages/nlme/indexhtml
Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
| Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Niinemets Ü, Walter A, Fiorani F, Schurr U (2010) A method to construct dose–response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data. Journal of Experimental Botany 61, 2043–2055.
| A method to construct dose–response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193, 30–50.
| Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control.Crossref | GoogleScholarGoogle Scholar |
Püschel D, Bitterlich M, Rydlová J, Jansa J (2020) Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae. Mycorrhiza 30, 299–313.
| Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae.Crossref | GoogleScholarGoogle Scholar |
Quilambo OA (2004) Review – The vesicular-arbuscular mycorrhizal symbiosis. African Journal of Biotechnology 2, 539–546.
| Review – The vesicular-arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2019) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria). Available at https://wwwR-projectorg/
Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23, 515–531.
| An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota).Crossref | GoogleScholarGoogle Scholar |
Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant and Soil 233, 167–177.
| Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils.Crossref | GoogleScholarGoogle Scholar |
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Current Opinion in Biotechnology 26, 115–124.
| Salt resistant crop plants.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Lozano JM, Azcón R (2000) Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity. Mycorrhiza 10, 137–143.
| Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity.Crossref | GoogleScholarGoogle Scholar |
Ryser P (1998) Intra- and interspecific variation in root length, root turnover and the underlying parameters. In ‘Inherent variation in plant growth physiological mechanisms and ecological consequences’. (Eds H Lambers, H Poorter, MMI Van Vuuren) pp. 441–465. (Backhuys Publishers: Leiden, The Netherlands)
Sannazzaro AI, Echeverría M, Albertó EO, Ruiz OA, Menéndez AB (2007) Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiology and Biochemistry 45, 39–46.
| Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza.Crossref | GoogleScholarGoogle Scholar |
Schüßler A, Walker C (2010) ‘The glomeromycota: a species list with new families and new genera.’ (Royal Botanic Garden Edinburgh: Gloucester, UK)
Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Critical Review in Plant Sciences 32, 237–249.
| Improving salinity tolerance in cereals.Crossref | GoogleScholarGoogle Scholar |
Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. Journal of Experimental Botany 55, 2343–2351.
| Root growth maintenance during water deficits: physiology to functional genomics.Crossref | GoogleScholarGoogle Scholar |
Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis.’ 3rd edn. (Academic Press: London, UK)
Solaiman Z (2014) Contribution of arbuscular mycorrhizal fungi to soil carbon sequestration. In ‘Mycorrhizal fungi: use in sustainable agriculture and land restoration. Soil Biology, Vol. 41’. (Eds Z Solaiman, L Abbott, A Varma) pp. 287–296. (Springer: Berlin, Heidelberg) https://doi.org/10.1007/978-3-662-45370-4_18
Stram DO (1996) Meta-analysis of published data using a linear mixed-effects model. Biometrics 52, 536–544.
| Meta-analysis of published data using a linear mixed-effects model.Crossref | GoogleScholarGoogle Scholar |
Tang L, Zhou QS, Gao Y, Li P (2022) Biomass allocation in response to salinity and competition in native and invasive species. Ecosphere 13, e3900
| Biomass allocation in response to salinity and competition in native and invasive species.Crossref | GoogleScholarGoogle Scholar |
Uchiya P, Escaray FJ, Bilenca D, Pieckenstain F, Ruiz OA, Menendez AB (2016) Salt effects on functional traits in model and in economically important Lotus species. Plant Biology 18, 703–709.
| Salt effects on functional traits in model and in economically important Lotus species.Crossref | GoogleScholarGoogle Scholar |
Valladares F, Sánchez-Gómez D (2006) Ecophysiological traits associated with drought in Mediterranean tree seedlings: individual responses versus interspecific trends in eleven species. Plant Biology 8, 688–697.
| Ecophysiological traits associated with drought in Mediterranean tree seedlings: individual responses versus interspecific trends in eleven species.Crossref | GoogleScholarGoogle Scholar |
van Noordwijk M, de Willigen P (1987) Agricultural concepts of roots: from morphogenetic to functional equilibrium between root and shoot growth. Netherlands Journal of Agricultural Science 35, 487–496.
| Agricultural concepts of roots: from morphogenetic to functional equilibrium between root and shoot growth.Crossref | GoogleScholarGoogle Scholar |
Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22, 227–235.
| Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010.Crossref | GoogleScholarGoogle Scholar |
Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional. Oikos 116, 882–892.
| Let the concept of trait be functional.Crossref | GoogleScholarGoogle Scholar |
Wang X-X, Li H, Chu Q, Feng G, Kuyper TW, Rengel Z (2020) Mycorrhizal impacts on root trait plasticity of six maize varieties along a phosphorus supply gradient. Plant and Soil 448, 71–86.
| Mycorrhizal impacts on root trait plasticity of six maize varieties along a phosphorus supply gradient.Crossref | GoogleScholarGoogle Scholar |
Weiner J (2003) Ecology – the science of agriculture in the 21st century. The Journal of Agricultural Science 141, 371–377.
| Ecology – the science of agriculture in the 21st century.Crossref | GoogleScholarGoogle Scholar |
Weiner J (2004) Allocation, plasticity and allometry in plants. Perspectives in Plant Ecology, Evolution and Systematics 6, 207–215.
| Allocation, plasticity and allometry in plants.Crossref | GoogleScholarGoogle Scholar |
Wickham H (2016) ‘Ggplot2: elegant graphics for data analysis.’ 2nd edn. p. 260. (Springer International Publishing: Cham, Switzerland)
Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science 10, 615–620.
| Developing salt-tolerant crop plants: challenges and opportunities.Crossref | GoogleScholarGoogle Scholar |
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.
| Effects of arbuscular mycorrhizal fungi on plant growth depend on root system: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
