Abstract
Background and aims
Plasticity of plants refers to their ability to produce different phenotypes in different environments. Plants show plasticity aboveground as well as belowground. The influence of the arbuscular mycorrhizal fungal (AMF) symbiosis on root plasticity is poorly known. This study aimed to quantify plasticity of root-system related, morphological, physiological or mycorrhizal traits along a soil phosphorus (P) supply gradient.
Methods
Six varieties of maize (Zea mays L.) were grown in pots with or without AMF at five rates of P supply. Fifteen root traits were measured and calculated after seven weeks of growth.
Results
Root system traits (biomass and length) and physiological traits (phosphatase activity at the root surface and in the rhizosphere) showed high plasticity along the P gradient, whereas morphological traits (specific root length and root diameter) exhibited low plasticity. Mycorrhizal presence reduced root-system plasticity (biomass and length), increased morphological-trait plasticity (specific root length and proportion of fine roots), but had little effects on other traits.
Conclusion
Our results indicate that trait plasticity related to the root system constitutes the most important adaptive strategy for maize to variation in P supply, and that the mycorrhizal symbiosis reduces root-system plasticity.
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References
Alvey S, Bagayoko M, Neumann G, Buerkert A (2001) Cereal/legume rotations affect chemical properties and biological activities in two West African soils. Plant Soil 231:45–54
An GH, Kobayashi S, Enoki H, Sonobe K, Muraki M, Karasawa T, Ezawa T (2010) How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant Soil 327:441–453
Bao SD (2000) Soil agrochemical analysis, 3rd edn. China Agriculture Press, Beijing, pp 1–495
Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699
Bayuelo-Jimenez JS, Gallardo-Valdez M, Perez-Decelis VA, Magdaleno-Armas L, Ochoa I, Lynch JP (2011) Genotypic variation for root traits of maize (Zea mays L.) from the Purhepecha Plateau under contrasting phosphorus availability. Field Crop Res 121:350–362
Callaway RM, Pennings SC, Richards CL (2003) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128
Chave M, Angeon V, Paut R, Collombet R, Tchamitchian M (2019) Codesigning biodiversity-based agrosystems promotes alternatives to mycorrhizal inoculants. Agron Sustain Dev 39:48
Chu Q (2013) The contribution of mycorrhizal pathway to p uptake efficiency of maize (Zea mays L.). Dissertation for Doctor Degree, China Agricultural University
Chu Q, Wang XX, Yang Y, Chen FJ, Zhang FS, Feng G (2013) Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza 23:497–505
Denison RF (2012) Darwinian agriculture: how understanding evolution can improve agriculture. Princeton University Press, Princeton, pp 1–258
Elsen A, Beeterens R, Swennen R, De Waele D (2003) Effects of an arbuscular mycorrhizal fungus and two plant-parasitic nematodes on Musa genotypes differing in root morphology. Biol Fert Soils 38:367–376
Farrar J, Gunn S (1998) Allocation: allometry, acclimation–and alchemy. In: Lambers H, Poorter H, van Vuren MMI (eds) Inherent variation in plant growth. Backhuys Publishers, Leiden, pp 183–197
Fort F, Cruz P, Catrice O, Delbrut A, Luzarreta M, Stroia C, Jouany C (2015) Root functional trait syndromes and plasticity drive the ability of grassland Fabaceae to tolerate water and phosphorus shortage. Environ Exp Bot 110:62–72
Freschet GT, Swart EM, Cornelissen JH (2015) Integrated plant phenotypic responses to contrasting above-and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytol 206:1247–1260
Galván GA, Kuyper TW, Burger K, Keizer LCP, Hoekstra RF, Kik C, Scholten OE (2011) Genetic analysis of the interaction between Allium species and arbuscular mycorrhizal fungi. Theor Appl Genet 122:947–960
Gao XP, Hoffland E, Stomph T, Grant CA, Zou CQ, Zhang FS (2012) Improving zinc bioavailability in transition from flooded to aerobic rice. A review. Agron Sustain Dev 32:465–478
Gutjahr C, Paszkowski U (2013) Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Front Plant Sci 4:204
Hao L, Zhang J, Christie P, Li X (2008) Response of two maize inbred lines with contrasting phosphorus efficiency and root morphology to mycorrhizal colonization at different soil phosphorus supply levels. J Plant Nutr 31:1059–1073
Hardy E, Blumenthal D (2008) An efficient and inexpensive system for greenhouse pot rotation. HortSci 43:965
Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisiton of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429
Hazard C, Johnson D (2018) Does genotypic and species diversity of mycorrhizal plants and fungi affect ecosystem function? New Phytol 220:1122–1128
Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat-varieties, landraces, and ancestors. Can J Bot 70:2032–2040
Hetrick BAD, Wilson GWT, Schwab AP (1994) Mycorrhizal activity in warm-season and cool-season grasses – variation in nutrient-uptake strategies. Can J Bot 72:1002–1008
Iversen CM, McCormack ML, Powell AS, Blackwood CB, Freschet GT, Kattge J, Roumet C, Stover DB, Soudzilovskaia NA, Valverde-Barrantes OJ (2017) A global fine-root ecology database to address below-ground challenges in plant ecology. New Phytol 215:15–26
Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular arbuscular mycorrhizal fungi associated with Trifolium subterraneum l. 2. Hyphal transport of 32P over defined distances. New Phytol 120:509–516
Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF (2000) Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci 40:358–364
Kitson R, Mellon M (1944) Colorimetric determination of phosphorus as molybdivanadophosphoric acid. Ind Eng Chem Anal Ed 16:379–383
Kramer-Walter KR, Laughlin DC (2017) Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation. Plant Soil 416:539–550
Kruger M, Kruger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot-Lond 98:693–713
Lambers H, Martinoia E, Renton M (2015) Plant adaptations to severely phosphorus-impoverished soils. Curr Opin Plant Biol 25:23–31
Li HG, Shen JB, Zhang FS, Marschner P, Cawthray G, Rengel Z (2010) Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil. Biol Fert Soils 46:79–91
Li H, Ma Q, Li H, Zhang F, Rengel Z, Shen J (2014) Root morphological responses to localized nutrient supply differ among crop species with contrasting root traits. Plant Soil 376:151–163
Li H, Liu B, McCormack ML, Ma Z, Guo D (2017) Diverse belowground resource strategies underlie plant species coexistence and spatial distribution in three grasslands along a precipitation gradient. New Phytol 216:1140–1150
Liu Y, Mi GH, Chen FJ, Zhang JH, Zhang FS (2004) Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Sci 167:217–223
Liu BT, Li HB, Zhu BA, Koide RT, Eissenstat DM, Guo DL (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol 208:125–136
Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot-Lond 112:347–357
Matesanz S, Milla R (2018) Differential plasticity to water and nutrients between crops and their wild progenitors. Environ Exp Bot 145:54–63
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518
Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol 181:950–959
Neumann G (2006) Quantitative determination of acid phosphatase activity in the rhizosphere and on the root surface. In: Luster J, Finlay R (eds) Handbook of methods used in Rhizosphere research. Swiss Federal Research Institute WSL, Birmensdorf
Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker M, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn A, Pronk A (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442
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 Phytol 193:30–50
Ryan M, Tibbett M, Edmonds-Tibbett T, Suriyagoda L, Lambers H, Cawthray G, Pang J (2012) Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant Cell Environ 35:2170–2180
Ryan MH, Kidd DR, Sandral GA, Yang ZJ, Lambers H, Culvenor RA, Stefanski A, Nichols PGH, Haling RE, Simpson RJ (2016) High variation in the percentage of root length colonised by arbuscular mycorrhizal fungi among 139 lines representing the species subterranean clover (Trifolium subterraneum). Appl Soil Ecol 98:221–232
Sadras VO, Denison RF (2016) Neither crop genetics nor crop management can be optimised. Field Crop Res 189:75–83
Semchenko M, Zobel K (2005) The effect of breeding on allometry and phenotypic plasticity in four varieties of oat (Avena sativa L.). Field Crop Res 93:151–168
Shen Q, Wen ZH, Dong Y, Li HG, Miao YX, Shen JB (2018) The responses of root morphology and phosphorus-mobilizing exudations in wheat to increasing shoot phosphorus concentration. AoB Plants 10:1–11
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic, New York, pp 1–769
Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057
Trouvelot A, Kough JL, Gianiazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un système radiculaire. Recherche de methodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological genetical aspects of Mycorrhizae. INRA Press, Paris, pp 217–221
Valverde-Barrantes OJ, Freschet GT, Roumet C, Blackwood CB (2017) A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants. New Phytol 215:1562–1573
Van der Heijden MGA (2002) Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search of underlying mechanisms and general principles. In: Van der Heijden MGA, Sanders I (eds) Mycorrhizal ecology. Ecological studies, vol 157. Springer, Berlin, pp 243–265
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447
Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197
Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560
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
Wang XX, Hoffland E, Feng G, Kuyper TW (2017) Phosphate uptake from phytate due to hyphae-mediated phytase activity by arbuscular mycorrhizal maize. Front Plant Sci 8:1–8
Wang R, Wang Q, Zhao N, Xu Z, Zhu X, Jiao C, Yu G, He N (2018a) Different phylogenetic and environmental controls of first-order root morphological and nutrient traits: evidence of multidimensional root traits. Funct Ecol 32:29–39
Wang XX, Wang XJ, Sun Y, Cheng Y, Liu ST, Chen XP, Feng G, Kuyper TW (2018b) Arbuscular mycorrhizal fungi negatively affect nitrogen acquisition and grain yield of maize in a N deficient soil. Front Microbiol 9:1–10
Wen Z, Li H, Shen J, Rengel Z (2017) Maize responds to low shoot P concentration by altering root morphology rather than increasing root exudation. Plant Soil 416:377–389
Yang Y (2009) Variation of phosphorus (P) efficiencies and mycorrhizal dependence of maize cultivars breeded in different years. Dissertation for Master Degree, China Agricultural University
Zabinski CA, Quinn L, Callaway RM (2002) Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct Ecol 16:758–765
Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:1–4
Zhang L, Xu MG, Liu Y, Zhang FS, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032
Zhang C, Simpson RJ, Kim CM, Warthmann N, Delhaize E, Dolan L, Byrne ME, Wu Y, Ryan PR (2018) Do longer root hairs improve phosphorus uptake? Testing the hypothesis with transgenic Brachypodium distachyon lines overexpressing endogenous RSL genes. New Phytol 217:1654–1666
Zheng CY, Zhang JL, Li XL (2013) Phosphorus supply level affects the regulation of phosphorus uptake by different arbuscular mycorrhizal fungal species in a highly P-efficient backcross maize line. Crop Pasture Sci 64:881–891
Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255
Zhu YG, Smith FA, Smith SE (2003) Phosphorus efficiencies and responses of barley (Hordeum vulgare L.) to arbuscular mycorrhizal fungi grown in highly calcareous soil. Mycorrhiza 13:93–100
Acknowledgements
This study was financially supported by National Key R&D Program of China (2017YFD0200200) and the National Natural Science Foundation of China (U1703232). We are grateful to four anonymous reviewers for their critical comments on an earlier version of this manuscript.
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Wang, XX., Li, H., Chu, Q. et al. Mycorrhizal impacts on root trait plasticity of six maize varieties along a phosphorus supply gradient. Plant Soil 448, 71–86 (2020). https://doi.org/10.1007/s11104-019-04396-0
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DOI: https://doi.org/10.1007/s11104-019-04396-0