Changes in climatic conditions drive variations in arbuscular mycorrhizal fungi diversity and composition in semi-arid oak forests

Nahid Jafarian, Javad Mirzaei, Reza Omidipour, Yahya Kooch

Journal of Forestry Research ›› 2024, Vol. 35 ›› Issue (1) : 94.

Journal of Forestry Research All Journals
PDF
Journal of Forestry Research ›› 2024, Vol. 35 ›› Issue (1) : 94. DOI: 10.1007/s11676-024-01744-4
Original Paper

Changes in climatic conditions drive variations in arbuscular mycorrhizal fungi diversity and composition in semi-arid oak forests

Author information +
History +

Abstract

Arbuscular mycorrhizal fungi (AMF) play a vital role in plant productivity and ecosystem functions. However, their responses to abiotic factors (i.e., climate, physiography, and soil properties) are unknown, especially across climatic gradients and slope aspects in arid and semi-arid ecosystems. In this study, using 60 composite soil samples, direct and indirect effects of climate factors and slope aspects on AMF diversity, composition and spore density were studied. The findings indicate that climate has a more direct influence on soil properties (P < 0.001) in comparison to slope aspect (P = 0.449). In contrast, climate significantly affected AMF diversity and composition, with the highest diversity in dryer areas. Soil pH had the highest correlation with different facets of AMF diversity. Structural equation modeling (SEM) indicated that only a small part of the variation in AMF diversity and spore density could be explained by climate characteristics, slope aspect and soil properties. Based on SEM results, climate was the most important determinant of AMF diversity and spore density; slope aspect had a less critical role. The outputs suggest that variations in AMF diversity are derived by the direct effects of climate and the indirect effect of soil chemical properties. In addition, with increasing dryness, sporulation and AMF diversity increased.

Graphical Abstract

Cite this article

Download citation ▾
Nahid Jafarian, Javad Mirzaei, Reza Omidipour, Yahya Kooch. Changes in climatic conditions drive variations in arbuscular mycorrhizal fungi diversity and composition in semi-arid oak forests. Journal of Forestry Research, 2024, 35(1): 94 https://doi.org/10.1007/s11676-024-01744-4
This is a preview of subscription content, contact us for subscripton.

References

AbbotLK, RobsonAD. Factors influence the occurrence of vesicular–arbuscular mycorrhizas. Agric Ecosys Environ, 1991, 35: 121-150
CrossRef Google scholar
AdenanS, OjaJ, AlataloJM, ShraimAM, AlsafranM, TedersooL, AhmedT. Diversity of arbuscular mycorrhizal fungi and its chemical drivers across dryland habitats. Mycorrhiza, 2021, 31: 685-697
CrossRef Google scholar
Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic Press, p 576. https://doi.org/10.1016/B978-0-12-513840-6.X5014-9
AlguacilMM, TorrecillasE, LozanoZ, TorresMP, RoldánA. Prunus persica crop management differentially promotes arbuscular mycorrhizal fungi diversity in a tropical agro-ecosystem. PLoS ONE, 2014, 9(2)
CrossRef Google scholar
Aminian NasabP, SedaqhatiE, HosseiniS, Saberi RisehR. Investigation of climate, soil physico-chemical properties and host on arbuscular mycorrhizal fungi activity in Rafsanjan. Biol Con Pes Plant Dis, 2021, 9(2): 216-197
CrossRef Google scholar
AndersonJP, DomschKH. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem, 1978, 10(3): 215-221
CrossRef Google scholar
Anderson MJ (2014) Permutational multivariate analysis of variance (PERMANOVA). Wiley statsref: statistics reference online, pp 1–15.
AugéRM. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza, 2001, 11(1): 3-42
CrossRef Google scholar
BainardLD, KochAM, GordonAM. Influence of trees on the spatial structure of arbuscular mycorrhizal communities in a temperate tree-based intercropping system. Agric Ecosyst Environ, 2011, 144: 13-20
CrossRef Google scholar
BentoRA, de NovaisCB, Saggin-JúniorOJ, de OliveiraLA, SampaioPDTB. Pioneer tree Bellucia imperialis (Melastomataceae) from central Amazon with seedlings highly dependent on arbuscular mycorrhizal fungi. J Fungi, 2023, 9(5): 540
CrossRef Google scholar
BordoloA, NathPC, ShuklaAK. Distribution of arbuscular mycorrhizal fungi associated with different land use systems of Arunachal Pradesh of Eastern Himalayan region. World J Microbiol Biotechnol, 2015, 10: 1587-1593
CrossRef Google scholar
BouyoucosGJ. Hydrometer method improved for making particle size analysis of soils. Agron J, 1962, 54: 464-465
CrossRef Google scholar
Bremner JM, Mulvaney CS (1982) Nitrogen−Total. In: Page AL (ed) Methods of soil analysis: part 2 chemical and microbiological properties, pp 595–624. https://doi.org/10.2134/agronmonogr9.2.2ed.c31
CalaçaFJS, BustamanteMMC. Richness of arbuscular mycorrhizal fungi (Glomeromycota) along a vegetation gradient of Brazilian Cerrado: responses to seasonality, soil types, and plant communities. Mycolo Prog, 2022, 21: 27
CrossRef Google scholar
CaravacaF, AlguacilM, BareaJ, RoldánA. Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosystem. Soil Biol Biochem, 2005, 37: 227-233
CrossRef Google scholar
CeulemansT, VanGM, JacquemynH, BoeraeveM, PlueJ, SaarL, KasariL, PeetersG, van AckerK, CrauwelsS. Arbuscular mycorrhizal fungi in European grasslands under nutrient pollution. Glob Ecol Biogeogr, 2019, 28: 1796-1805
CrossRef Google scholar
ChaiYX, JiangSJ, GuoWJ, QinMS, PanJB, BahadurA, ShiGX, LuoJJ, JinZC, LiuYJ, ZhangQ, AnLZ, FengHY. The effect of slope aspect on the phylogenetic structure of arbuscular mycorrhizal fungal communities in an alpine ecosystem. Soil Biol Biochem, 2018, 126: 103-113
CrossRef Google scholar
ChaudharyVB, CuencaG, JohnsonNC. Tropical temperate comparison of landscape-scale arbuscular mycorrhizal fungal species distributions. Divers Distrib, 2018, 24: 116-128
CrossRef Google scholar
Choudhary BK, Ali khan M, Saxena KG (2010) Mycorrhizal spore density in relation to physico-chemical properties of soil: a case study of central Himalaya. Maejo Int J Sci Technol 5:243–251. https://www.researchgate.net/publication/294292917
ChourasiyaD, GuptaMM, SahniS, OehlF, AgnihotriR, BuadeR, MaheshwariH, PrakashA, SharmaMP. Unraveling the AM fungal community for understanding its ecosystem resilience to changed climate in agroecosystems. Symbiosis, 2021, 84(3): 295-310
CrossRef Google scholar
Da SilvaIR, de MelloCMA, NetoRAF, da SilvaDKA, MeloALd, OehlF, MaiaLC. Diversity of arbuscular mycorrhizal fungi along an environmental gradient in the Brazilian semiarid. Appl Soil Ecol, 2014, 84: 166-175
CrossRef Google scholar
DhumalKC, ShindeBP. Impact of chemical properties of soil on spore density, colonization, and distribution of native arbuscular mycorrhizal fungi associated with Capsicum annuum L. J Appl Biolo Biotech, 2020, 8(5): 59-67
CrossRef Google scholar
Dickie IA, Martinez-Garcia LB, Koele N, Grelet GA, Tylianakis JM, Peltzer DA, Richardson SJ (2013) Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant Soil 367:11–39. https://www.jstor.org/stable/42952876
DumbrellAJ, NelsonM, HelgasonT, DythamC, FitterAH. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J, 2010, 4: 337-345
CrossRef Google scholar
DumbrellAJ, AshtonPD, AzizN, FengG, NelsonM, DythamC, FitterAH, HelgasonT. Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol, 2011, 190: 794-804
CrossRef Google scholar
FaggioliVS, CovacevichF, GrilliG, LorenzonC, AimettaB, SagadinM, CabelloMN. Environmental response of arbuscular mycorrhizal fungi under soybean cultivation at a regional scale. Mycorrhiza, 2022, 32(5–6): 425-438
CrossRef Google scholar
FitzsimonsMS, MillerRM, JastrowJD. Scale-dependent niche axes of arbuscular mycorrhizal fungi. Oecologia, 2008, 158: 117-127
CrossRef Google scholar
GavitoME, CurtisPS, MikkelsenTN, JakobsenI. Atmospheric CO2 and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (Pisum sativum L.) plants. J Exp Bot, 2000, 51(352): 1931-1938
CrossRef Google scholar
Gutierrez-JuradoHA, VivoniER, HarrisonJBJ, GuanH. Ecohydrology of root zone water fluxes and soil development in complex semiarid rangelands. Hydrol Process, 2006, 20: 3289-3316
CrossRef Google scholar
HodgeA, StorerK. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil, 2015, 386: 1-19
CrossRef Google scholar
HolmgrenM, StappP, DickmanCR, GraciaC, GrahamS, GutiérrezJR, SqueoFA. Extreme climatic events shape arid and semiarid ecosystems. Fron Ecol Environ, 2006, 4(2): 87-95
CrossRef Google scholar
HopkinsJR, BennettAE. Spore traits mediate disturbance effects on arbuscular mycorrhizal fungal community composition and mutualisms. Ecology, 2023, 104(5)
CrossRef Google scholar
HopmansJW, QureshiAS, KisekkaI, MunnsR, GrattanSR, RengasamyP, TaleisnikE. Critical knowledge gaps and research priorities in global soil salinity. Adv Agron, 2021, 169: 1-191
CrossRef Google scholar
IslamMN, GermidaJJ, WalleyFL. Responses of arbuscular mycorrhizal fungal communities to soil core transplantation across Saskatchewan prairie climatic regions. Can J Soil Sci, 2019, 100(1): 81-96
CrossRef Google scholar
JafarianN, MirzaeiJ, OmidipourR, KoochY. Effects of micro-climatic conditions on soil properties along a climate gradient in oak forests, west of Iran: Emphasizing phosphatase and urease enzyme activity. CATENA, 2023, 224
CrossRef Google scholar
JiB, BeverJD. Plant preferential allocation and fungal reward decline with soil phosphorus enrichment: implications for mycorrhizal mutualism. Ecosphere, 2016, 7(5)
CrossRef Google scholar
JiB, BentivengaSP, CasperBB. Comparisons of AM fungal spore communities with the same hosts but different soil chemistries over local and geographic scales. Oecologia, 2012, 168: 187-197
CrossRef Google scholar
JohnsonNC, GrahamJD, SmithFA. Functioning of mycorrhizal association along the mutualism–parasitism continuum. New Phytol, 1997, 135: 575-586
CrossRef Google scholar
KandelerE, GerberH. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils, 1988, 6: 68
CrossRef Google scholar
Kojima T, Jenkins S, Weerasekara A, Fan JW (2014) Arbuscular mycorrhizal diversity and function in grassland ecosystems. In: Mycorrhizal fungi: use in sustainable agriculture and land restoration, pp 149–169. https://doi.org/10.1007/978-3-662-45370-4_9
LegendreP, LegendreL. Numerical ecology, 2012 3 Amsterdam Elsevier 853
LiXL, ZhangJL, GeorgeE, MarchnerH. Phosphorus acquisition from compacted soil by hyphae of a mycorrhizal fungus associated with red clover (Trifolium pratence). Can J Bot, 1997, 75(5): 723-729
CrossRef Google scholar
LiXL, ZhuTY, PengF, ChenQ, LinS, ChristieP, ZhangJL. Inner Mongolian steppe arbuscular mycorrhizal fungal communities respond more strongly to water availability than to nitrogen fertilization. Environ Microbiol, 2015, 17(8): 3051-3068
CrossRef Google scholar
LiC, WangRH, NingHS, LuoQH. Changes in climate extremes and their impact on wheat yield in Tianshan Mountains region, northwest China. Environ Earth Sci, 2016, 75: 1-13
CrossRef Google scholar
LiZJ, LiZY, TongXZ, ZhangJH, DongL, ZhengY, MaWH, ZhaoLQ, WangLX, WenL, DangZH, TuvshintogtokhI, LiangCZ, LiFYH. Climatic humidity mediates the strength of the species richness–biomass relationship on the Mongolian Plateau steppe. Sci Total Environ, 2020, 718
CrossRef Google scholar
LimaneA, SaadounN. Taxonomic diversity and morphological types of arbuscular mycorrhizal fungal communities symbiotic with Atlas pistachio along an aridity gradient in Algeria. Environ Exp Biol, 2022, 20(2): 119-126
CrossRef Google scholar
LiuM, ZhengR, BaiSL, BaiYE, WangJG. Slope aspect influences arbuscular mycorrhizal fungus communities in arid ecosystems of the Daqingshan Mountains, Inner Mongolia, North China. Mycorrhiza, 2016, 27: 189-200
CrossRef Google scholar
LiuD, LiuGH, ChenL, WangJT, ZhangLM. Soil pH determines fungal diversity along an elevation gradient in Southwestern China. Sci China Life Sci, 2017, 61(6): 718-726
CrossRef Google scholar
LiuRC, XiaoZY, HashemA, AbdAllahEF, WuQS. Mycorrhizal fungal diversity and its relationship with soil properties in Camellia oleifera. Agriculture, 2021, 11(6): 470
CrossRef Google scholar
Mahecha-VásquezG, SierraS, PosadaR. Diversity indices using arbuscular mycorrhizal fungi to evaluate the soil state in banana crops in Colombia. Appl Soil Ecol, 2017, 109: 32-39
CrossRef Google scholar
ManimegalaiV, SelvarajT, AmbikapathyV. Studies on isolation and identification of VAM fungi in Solanumviarum dunal of medicinal plants. Pelagia Res Library, 2011, 2: 621-628
MarshnerH, DellB. Nutrient uptake in mycorrhizal symbiosis. Plant Soil, 1996, 159: 89-102
CrossRef Google scholar
MedinaA, AzcónR. Effectiveness of the application of arbuscular mycorrhiza fungi and organic amendments to improve soil quality and plant performance under stress conditions. J Soil Sci Plant Nutr, 2010, 10(3): 354-372
CrossRef Google scholar
MengeJA, SteirleO, BagyarajDJ, JohnsonELV, LeonardRT. Phosphorus concentration in plant responsible for inhibition of mycorrhizal infection. New Phytol, 1978, 85: 575-578
CrossRef Google scholar
MirzaeiJ, MoradiM. Biodiversity of arbuscular mycorrhizal fungi in Amygdalus scoparia Spach plantations and a natural stand. J for Res, 2017, 28(6): 1209-1217
CrossRef Google scholar
MirzaeiJ, HeydariM, OmidipourR, JafarianN, CarcailletC. Decrease in soil functionalities and herbs’ diversity, but not that of arbuscular mycorrhizal fungi, linked to short fire interval in semi-arid oak forest ecosystem, west Iran. Plants, 2023, 12(5): 1112
CrossRef Google scholar
Montiel-RozasMDM, Lopez-GarciaA, MadejonP, MadejonE. Native soil organic matter as a decisive factor to determine the arbuscular mycorrhizal fungal community structure in contaminated soils. Biol Fertil Soils, 2017, 53: 327-338
CrossRef Google scholar
Moradi BehbahaniS, MoradiM, BasiriR, MirzaeiJ. Sand mining disturbances and their effects on the diversity of arbuscular mycorrhizal fungi in a riparian forest of Iran. J Arid Land, 2017, 9(6): 837-849
CrossRef Google scholar
MorenoG, ObradorJJ, GarciaA. Impact of evergreen oaks on soil fertility and crop production in intercropped dehesas. Agric Ecosyst Environ, 2007, 119: 270-280
CrossRef Google scholar
MythiliM, RamalakshmiA. Unraveling the distribution of AMF communities and their metabolites associated with soils of minor millets. Rhizosphere, 2022, 21
CrossRef Google scholar
OehlF, Da SilvaGA, GotoBT, MaiaLC, SieverdingE. Glomeromycota: two new classes and a new order. Mycotaxon, 2011, 116(1): 365-379
CrossRef Google scholar
OhlingerR. SchinnerF, KandelerE, OhlingerR, MargesinR. Dehydrogenase activity with the substrate TTC. Methods in soil biology, 1996 Berlin Springer 246-265
OksanenJ, BlanchetFG, FriendlyM, KindtR, LegendreP, McGlinnD, MinchinPR, O’hara RB, Simpson GL, Solymos P, Stevens MHH, . Vegan: community ecology package. R Package Version, 2022, 2(5-7): 2020
OliverioAM, BradfordMA, FiererN. Identifying the microbial taxa that consistently respond to soil warming across time and space. Glob Chang Biol, 2017, 23: 2217-2129
CrossRef Google scholar
OlsenSR, ColeCV, WatanabeFS, DeanLA. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular, 1954, 939: 1-19
PelliconeG, CaloieroT, CaloieroI. The De Martonne aridity index in Calabria (Southern Italy). J Maps, 2019, 15(2): 788-796
CrossRef Google scholar
Pielou, . The measurement of diversity in different types of biological collections. J Theoretic Biol, 1966, 13: 131-144
CrossRef Google scholar
PropsterJR, JohnsonNC. Uncoupling the effects of phosphorus and precipitation on arbuscular mycorrhizas in the Serengeti. Plant Soil, 2015, 388: 21-34
CrossRef Google scholar
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
RasmussenPU, HugerthLW, BlanchetFG, AnderssonAF, LindahlBD, TackAJ. Multiscale patterns and drivers of arbuscular mycorrhizal fungal communities in the roots and root-associated soil of a wild perennial herb. New Phytol, 2018, 220(4): 1248-1261
CrossRef Google scholar
RazoukR, KajjiA. Effect of arbuscular mycorrhizal fungi on water relations and growth of young plum trees under severe water stress conditions. Int J Plant Soil Sci, 2015, 5(5): 10
CrossRef Google scholar
RossJP. Effect of nontreated field soil on sporulation of vesicular–arbuscular mycorrhizal fungi associated with soybean. J Phytopathol, 1980, 70: 100-105
RotenbergE, YakirD. Contribution of semi-arid forests to the climate system. Science, 2010, 327: 451-454
CrossRef Google scholar
SacoP, WillgooseG, HancockG. Eco-geomorphology of banded vegetation patterns in arid and semi-arid regions. Hydrol Earth Sci, 2007, 11: 1717-1730
CrossRef Google scholar
SchenckNC, PerezY. Manual for the identification of VA mycorrhizal fungi, 1990 Gainesville Synergistic Publications
SchroderNV. Temperature response of Endogone mycorrhiza on soybean roots. Mycologia, 1974, 66(4): 600-605
CrossRef Google scholar
SedaghatiE, YazdanpanahM, NadiM. A review of taxonomic studies of arbuscular mycorrhizal fungi in Iran. Mycol Iran, 2021, 8(2): 15-30
CrossRef Google scholar
ShannonCE, WeaverW. The mathematical theory of communications, 1963 Urbana University of Illinois Press 125
SimpsonEH. Measurement of diversity. Nature, 1949, 163: 688
CrossRef Google scholar
SmithSE, ReadDJ. Mycorrhizal symbiosis, 2008 3 New York Academic press 694
Solís-RodríguezURJ, Ramos-ZapataJA, Hernández-CuevasL, Salinas-PebaL, GuadarramaP. Arbuscular mycorrhizal fungi diversity and distribution in tropical low flooding forest in Mexico. Mycol Prog, 2020, 19: 195-204
CrossRef Google scholar
SotiP, KariyatR, RacelisA. Effective farm management promotes native AMF and benefit organic farming systems. Agric Ecosy Environ, 2023, 342
CrossRef Google scholar
TresederKK, MackMC, CrossA. Relationships among fires, fungi, and soil dynamics in Alaskan boreal forests. Ecol Appl, 2004, 14: 1826-1838
CrossRef Google scholar
VanceED, BrookesPC, JenkinsonDS. An extraction method for measuring soil microbial biomass C. Soil Biol Bioch, 1987, 19(6): 703-707
CrossRef Google scholar
VarmaA. Mycorrhiza, 2008 Uttar Pradesh India Amity University 29-57
CrossRef Google scholar
VerbruggenE, van der HeijdenMGA, WeedonJT, KowalchuckGA, RolingWFM. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Ecology, 2012, 12: 2341-2353
CrossRef Google scholar
WahabA, MuhammadM, MunirA, AbdiG, ZamanW, AyazA, ReddySPP. Role of arbuscular mycorrhizal fungi in regulating growth, enhancing productivity, and potentially influencing ecosystems under abiotic and biotic stresses. Plants, 2023, 12(17): 3102
CrossRef Google scholar
WalkleyA, BlackIA. an examination of the Degetiareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci, 1934, 37: 29-38
CrossRef Google scholar
WangF. Occurrence of arbuscular mycorrhizal fungi in mining-impacted sites and their contribution to ecological restoration: mechanisms and applications. Crit Rev Environ Sci Technol, 2017, 47(20): 1901-1957
CrossRef Google scholar
WangYS, LiuRJ. A checklist of arbuscular mycorrhizal fungi in the recent taxonomic system of Glomeromycota. Mycosystema, 2017, 36(7): 820-850
CrossRef Google scholar
WangJC, WangJ, HeJZ, ZhuYG, QiaoNH, GeY. Arbuscular mycorrhizal fungi and plant diversity drive restoration of nitrogen-cycling microbial communities. Mol Ecol, 2021, 30(16): 4133-4146
CrossRef Google scholar
WangJL, ZhangJW, WangCJ, RenGL, YangYR, WangDL. Precipitation exerts a strong influence on arbuscular mycorrhizal fungi community and network complexity in a semiarid steppe ecosystem. Eur J Soil Biol, 2021, 102
CrossRef Google scholar
WeijtmansK, DavisM, ClintonP, KuyperTW, GreenfieldL. Occurrence of arbuscular mycorrhiza and ectomycorrhizas on Leptospermum the Rakia catchment. Canterbury N Z J Ecol, 2007, 31(2): 255-260
XiangD, VerbruggenE, HuYJ, VeresoglouSD, RilligMC, ZhouWP, XuTL, LiH, HaoZP, ChenYL, ChenBD. Land use influences arbuscular mycorrhizal fungal communities in the farming–pastoral ecotone of northern China. New Phytol, 2014, 204: 968-978
CrossRef Google scholar
XuXL, WangXJ, ClearyM, WangP, LuNN, SunYJ, RönnbergJ. Slope position rather than thinning intensity affects arbuscular mycorrhizal fungi (AMF) community in Chinese fir plantations. Forests, 2020, 11: 273
CrossRef Google scholar
XueR, YangQ, MiaoFH, WangXZ, ShenYY. Slope aspect influences plant biomass, soil properties and microbial composition in alpine meadow on the Qinghai-Tibetan plateau. J Soil Sci Plant Nutr, 2018, 18(1): 1-12
CrossRef Google scholar
YanPX, HouH, LvYZ, ZhangHY, LiJ, ShaoLL, XieQM, LiangYL, LiJY, NiXL. Diversity characteristics of arbuscular mycorrhizal fungi communities in the soil along successional altitudes of Helan Mountain, arid, and semi-arid regions of China. Front Microbiol, 2023, 14: 1099131
CrossRef Google scholar
ZhangMG, YangM, ShiZY, GaoJK, WangXG. Biodiversity and variations of arbuscular mycorrhizal fungi associated with roots along elevations in Mt. Taibai of China. Diversity, 2022, 14(8): 626
CrossRef Google scholar
PDF

Accesses

Citations

1

Altmetric

Detail

Sections
Recommended

/