Arbuscular Mycorrhizal Fungi Compete Asymmetrically for Amino Acids with Native and Invasive Solidago.
Amino acid N source
Growth advantage
Path modeling
Plant invasion
Soil microbes
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
Jul 2022
Jul 2022
Historique:
received:
28
02
2021
accepted:
05
08
2021
pubmed:
19
8
2021
medline:
7
7
2022
entrez:
18
8
2021
Statut:
ppublish
Résumé
Arbuscular mycorrhizal fungi (AMF) and soil amino acids both affect plant performance. However, little is known about how AMF compete for amino acids with native and invasive congeners. We conducted a factorial experiment (inoculation, native and invasive species, and amino acids) to examine the competition for amino acids between soil microbes and both native and invasive congeners. The competition for amino acids between AMF and invasive Solidago canadensis was weaker than that observed between AMF and native S. decurrens. This asymmetric competition increased the growth advantage of S. canadensis over S. decurrens. The efficacy (biomass production per unit of nitrogen supply) of amino acids compared to ammonium was smaller in S. canadensis than in S. decurrens when both species were grown without inoculation, but the opposite was the case when both species were grown with AMF. AMF and all microbes differentially altered four phenotypic traits (plant height, leaf chlorophyll content, leaf number, and root biomass allocation) and the pathways determining the effects of amino acids on growth advantages. These findings suggest that AMF could enhance plant invasiveness through asymmetric competition for amino acids and that amino acid-driven invasiveness might be differentially regulated by different microbial guilds.
Identifiants
pubmed: 34406446
doi: 10.1007/s00248-021-01841-5
pii: 10.1007/s00248-021-01841-5
doi:
Substances chimiques
Amino Acids
0
Soil
0
Nitrogen
N762921K75
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
131-140Subventions
Organisme : National Natural Science Foundation of China
ID : 31971552
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273
pubmed: 17822399
Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. John Wiley & Sons, New York
Catford JA, Jasson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40
Yu HW, Yang JX, Gao Y, He WM (2016) Soil organic nitrogen endows invasive Solidago canadensis with greater advantages in low-phosphorus conditions. Ecosphere 7(3):e01254
Dong LJ, Ma LN, He WM (2021) Arbuscular mycorrhizal fungi help explain invasion success of Solidago canadensis. Appl Soil Ecol 157:103763.
Hu B, Chu C (2020) Nitrogen–phosphorus interplay: old story with molecular tale. New Phytol 225:1455–1460
pubmed: 31400226
Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142
pubmed: 17922835
Czaban W, Jämtgård S, Näsholm T, Rasmussen J, Nicolaisen M, Fomsgaard IS (2016) Direct acquisition of organic N by white clover even in the presence of inorganic N. Plant Soil 407:91–107
Lipson D, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316
pubmed: 24549899
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48
pubmed: 19210725
Warren CR (2014) Organic N molecules in the soil solution: what is known, what is unknown and the path forwards. Plant Soil 375:1–19
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants-an important N uptake pathway? Soil Biol Biochem 37:413–423
Yu HW, He WM (2021) Plant invaders outperform congeneric natives on amino acids. Basic Appl Ecol 54:75–84
Menzel A, Hempel S, Klotz S, Moora M, Pyšek P, Rillig MC, Zobel M, Kühn I (2017) Mycorrhizal status helps explain invasion success of alien plant species. Ecology 98:92–102
pubmed: 27935020
Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715
van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310
pubmed: 18047587
Jin L, Gu YJ, Xiao M, Chen J, Li B (2004) The history of Solidago canadensis invasion and the development of its mycorrhizal associations in newly-reclaimed land. Funct Plant Biol 31:979–986
pubmed: 32688966
Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186
Shen K, Cornelissen JHC, Wang Y, Wu C, He Y, Ou J, Tan Q, Xia T, Kang L, Guo Y, Wu B (2020) AM fungi alleviate phosphorus limitation and enhance nutrient competitiveness of invasivie plants via mycorrhizal networks in Karst areas. Front Ecol Evol 8:125
Stanescu S, Maherali H (2017) Arbuscular mycorrhizal fungi alter the competitive hierarchy along old-field plant species. Oecologia 183:479–491
pubmed: 27848080
Chen E, Liao H, Chen B, Peng S (2020) Arbuscular mycorrhizal fungi are a double-edged sword in plant invasion controlled by phosphorus concentration. New Phytol 226:295–300
pubmed: 31808168
Sun ZK, He WM (2018) Invasive Solidago canadensis versus its new and old neighbors: their competitive tolerance depends on soil microbial guilds. Flora 248:43–47
Harrison KA, Bol R, Bardgett RD (2008) Do plant species with different growth strategies vary in their ability to compete with soil microbes for chemical forms of nitrogen? Soil Biol Biochem 40:228–237
Hill PW, Jones DL (2019) Plant-microbe competition: does injection of isotopes of C and N into the rhizosphere effectively characterise plant use of soil N? New Phytol 221:796–806
pubmed: 30196574
Smith SE, Read DJ (2007) Mycorrhizal symbiosis. Academic Press, London
Okada T, Matsubara Y (2012) Tolerance to fusarium root rot and the changes in free amino acid contents in mycorrhizal asparagus plants. HortScience 47:751–754
Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic–nitrogen inputs to temperate grasslands. Ecology 84:1277–1287
Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143
pubmed: 21238010
Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanism and ecological relevance. New Phytol 198:656–669
pubmed: 23521345
Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, Wang E (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–1175
pubmed: 28596307
Morel MA, Castro-Sowinski S (2013) The complex molecular signaling network in microbe-plant interaction. In: Arora NK (ed) Plant microbe symbiosis: fundamentals and advances. Springer, New York, pp 169–199
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
pubmed: 21391813
Weber E (2003) Invasive plant species of the world: a reference guide to environmental weeds. CABI Publishing, Oxon, UK
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70
pubmed: 11986666
Liang MX, Liu XB, Etienne RS, Huang FM, Wang YF, Yu SX (2015) Arbuscular mycorrhizal fungi counteract the Janzen-Connell effect of soil pathogens. Ecology 96:562–574
pubmed: 26240876
Heinze J, Sitte M, Schindhelm A, Wright J, Joshi J (2016) Plant–soil feedbacks: a comparative study on the relative importance of soil feedbacks in the greenhouse versus the field. Oecologia 181:559–569
pubmed: 26922335
Thornton B, Robinson D (2005) Uptake and assimilation of nitrogen from solutions containing multiple N sources. Plant Cell Environ 28:813–821
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
Pinheiro J, Bates D, DebRoy S, Sarkar D (2017) nlme: linear and nonlinear mixed effects models. R package version 3:1–131
Sanchez G (2013) PLS path modeling with R. Trowchez Editions, Berkeley
Sanchez G, Trinchera L, Russolillo G (2017) plspm: tools for partial least squares path modeling (PLS–PM). R package version 0.4.9.
R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and the rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem 33:651–657
Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53
pubmed: 29120059
Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383
Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, pp. 147–168.
Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081
pubmed: 17460672
van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245
pubmed: 20002494
Baldrich P, Meyers BC (2019) Bacteria send messages to colonize plant roots. Science 365:868–869
pubmed: 31467211
Zhang P, Nie M, Li B, Wu J (2017) The transfer and allocation of newly fixed C by invasive Spartina alterniflora and native Phragmites australis to soil microbiota. Soil Biol Biochem 113:231–239
Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894
pubmed: 15347793
pmcid: 523350
Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Sign Behav 4:701–712
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. Febs Lett 581:2281–2289
pubmed: 17466985
Noll L, Zhang S, Wanek W (2019) Novel high-throughput approach to determine key processes of soil organic nitrogen cycling: gross protein depolymerization and microbial amino acid uptake. Soil Biol Biochem 130:73–81
pubmed: 31579309
Persson J, Näsholm T (2001) Amino acid uptake: a widespread ability among boreal forest plants. Ecol Lett 4:434–438