Abstract
Background and aims
Plant interactions with soil microbes are important drivers of biodiversity and dynamics of alpine plant communities. However, little is known about the effects of these interactions on seed germination and plant establishment of alpine plants under global climate change. We investigated the individual and interactive effects of warming, soil microbes and shrubs on seed germination, survival, and growth of herbaceous species.
Methods
We simulated warming and manipulated live and sterile soil microbes and microhabitat in the alpine meadow ecosystem dominated by the shrub (Dasiphora fruticosa) on the Qinghai-Tibet Plateau. We tested the interactive effects of warming, soil microbes, and shrubs on the germination, early life survival, and growth of herbaceous species. Soil microbial communities were determined by high-throughput sequencing.
Results
Our results showed that seed germination was significantly reduced under warming; seed germination was higher in live soils than in sterile soils; early life survival was lower under shrub canopies. Additionally, in the warming treatment, the positive effect of soil microbes on seed germination shifted to negative on the early survival of herbaceous species. Furthermore, in the warming treatment, shrubs enhanced the positive effects of soil microbes on seed germination and reduced the negative effects of soil microbes on early survival. The effects of these individual and interactive factors on herbaceous species also depended on species identity and life stages.
Conclusion
Overall, our work demonstrates that soil microbes were particularly critical at seed germination stage and plant interactions with soil microbes were significantly altered with experimental warming.
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Data availability
The datasets are available from corresponding authors upon reasonable request and the Gene sequencing data can be found in the: http://www.ncbi.nlm.nih.gov/bioproject/PRJNA911959.
References
Adler PB, Smull D, Beard KH et al (2018) Competition and coexistence in plant communities: intraspecific competition is stronger than interspecific competition. Ecol Lett 21:1319–1329. https://doi.org/10.1111/ele.13098
Al-Namazi AA, El-Bana MI, Bonser SP (2017) Competition and facilitation structure plant communities under nurse tree canopies in extremely stressful environments. Ecol Evol 7:2747–2755. https://doi.org/10.1002/ece3.2690
Anthelme F, Cavieres LA, Dangles O (2014) Facilitation among plants in alpine environments in the face of climate change. Front Plant Sci 5:1–16. https://doi.org/10.3389/fpls.2014.00387
Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: A new comparative index. Ecology 85:2682–2686. https://doi.org/10.1890/03-0650
Bao S (2000) Soil Agro-Chemistrical Analysis. Chinese Agricultural Press, Beijing in Chinese
Banerjee S, Kirkby CA, Schmutter D et al (2016) Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol Biochem 97:188–198. https://doi.org/10.1016/j.soilbio.2016.03.017
Baskin CC, Zackrisson O, Baskin JM (2002) Role of warm stratification in promoting germination of seeds of Empetrum hermaphroditum (Empetracea), a circumboreal species with a stony endocarp. Am J Bot 89:486–493. https://doi.org/10.3732/ajb.89.3.486
Baskin JM, Baskin CC (1972) Influence of Germination Date on Survival and Seed Production in a Natural Population of Leavenworthia stylosa. Am Midl Nat 88:318. https://doi.org/10.2307/2424357
Bauer JT (2019) When and where plant-soil feedback may promote plant coexistence : a meta-analysis. Ecol Lett. https://doi.org/10.1111/ele.13278
Benech-Arnold RL, Sánchez RA, Forcella F et al (2000) Environmental control of dormancy in weed seed banks in soil. F Crop Res 67:105–122. https://doi.org/10.1016/S0378-4290(00)00087-3
Bennett JA, Klironomos J (2019) Mechanisms of plant–soil feedback: interactions among biotic and abiotic drivers. New Phytol 222:91–96. https://doi.org/10.1111/nph.15603
Bennett JA, Maherali H, Reinhart KO et al (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 69:381–386
Bever JD (2003) Soil community feedback and the coexistence of competitors: Conceptual frameworks and empirical tests. New Phytol 157:465–473. https://doi.org/10.1046/j.1469-8137.2003.00714.x
Bever JD, Dickie IA, Facelli E et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478. https://doi.org/10.1016/j.tree.2010.05.004
Billingsley Tobias T, Farrer EC, Rosales A et al (2017) Seed-associated fungi in the alpine tundra: Both mutualists and pathogens could impact plant recruitment. Fungal Ecol 30:10–18. https://doi.org/10.1016/j.funeco.2017.08.001
Bragazza L, Parisod J, Buttler A, Bardgett RD (2013) Biogeochemical plant-soil microbe feedback in response to climate warming in peatlands. Nat Clim Chang 3:273–277. https://doi.org/10.1038/nclimate1781
Brigitta E, Ruth NS, Eckart W (2008) Colonization processes on a central alpine glacier foreland. J Veg Sci 19:855–862. https://doi.org/10.3170/2008-8-18464
Brooks ME, Kristensen K, van Benthem KJ et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400 https://doi.org/10.32614/rj-2017-066
Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, Dordrecht
Cavieres LA, Sierra-Almeida A (2012) Facilitative interactions do not wane with warming at high elevations in the Andes. Oecologia 170:575–584. https://doi.org/10.1007/s00442-012-2316-x
Cochrane JA, Hoyle GL, Yates CJ et al (2015) Climate warming delays and decreases seedling emergence in a Mediterranean ecosystem. Oikos 124:150–160. https://doi.org/10.1111/oik.01359
Cui H, Wagg C, Wang X et al (2022) The loss of above- and belowground biodiversity in degraded grasslands drives the decline of ecosystem multifunctionality. Appl Soil Ecol 172:104370 https://doi.org/10.1016/j.apsoil.2021.104370
Dai Z, Yu M, Chen H et al (2020) Elevated temperature shifts soil N cycling from microbial immobilization to enhanced mineralization, nitrification and denitrification across global terrestrial ecosystems. Glob Chang Biol 26:5267–5276. https://doi.org/10.1111/gcb.15211
David AS, Thapa-Magar KB, Afkhami ME (2018) Microbial mitigation–exacerbation continuum: a novel framework for microbiome effects on hosts in the face of stress. Ecology 99:517–523. https://doi.org/10.1002/ecy.2153
David AS, Thapa-Magar KB, Menges ES et al (2020) Do plant–microbe interactions support the Stress Gradient Hypothesis? Ecology 101:1–10
de Kroon H, Hendriks M, van Ruijven J et al (2012) Root responses to nutrients and soil biota: Drivers of species coexistence and ecosystem productivity. J Ecol 100:6–15. https://doi.org/10.1111/j.1365-2745.2011.01906.x
Defossez E, Courbaud B, Marcais B et al (2011) Do interactions between plant and soil biota change with elevation? A study on Fagus sylvatica. Biol Lett 7:699–701. https://doi.org/10.1098/rsbl.2011.0236
Delshadi S, Ebrahimi M, Shirmohammadi E (2017) Effectiveness of plant growth promoting rhizobacteria on Bromus tomentellus Boiss seed germination, growth and nutrients uptake under drought stress. S Afr J Bot 113:11–18. https://doi.org/10.1016/j.sajb.2017.07.006
Duponnois R, Ouahmane L, Kane A et al (2011) Nurse shrubs increased the early growth of Cupressus seedlings by enhancing belowground mutualism and soil microbial activity. Soil Biol Biochem 43:2160–2168. https://doi.org/10.1016/j.soilbio.2011.06.020
Edgar RC (2013) UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Eldridge DJ, Travers SK, Val J et al (2021) Experimental evidence of strong relationships between soil microbial communities and plant germination. J Ecol 109:2488–2498. https://doi.org/10.1111/1365-2745.13660
Ellis RH, Roberts EH (1980) The influence of temperature and moisture on seed viability period in barley (Hordeum distichum L.). Ann Bot 45:31–37. https://doi.org/10.1093/oxfordjournals.aob.a085798
Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, Cambridge
Fei S, Desprez JM, Potter KM et al (2017) Divergence of species responses to climate change. Sci Adv 3 https://doi.org/10.1126/sciadv.1603055
Fox J, Weisberg S (2011) Multivariate Linear Models in R. R Dev Core Team 31
Fraser RH, Lantz TC, Olthof I et al (2014) Warming-Induced Shrub Expansion and Lichen Decline in the Western Canadian Arctic. Ecosystems 17:1151–1168. https://doi.org/10.1007/s10021-014-9783-3
Geange SR, Holloway-Phillips MM, Briceño VF, Nicotra AB (2020) Aciphylla glacialis mortality, growth and frost resistance: A field warming experiment. Aust J Bot 67:599–609. https://doi.org/10.1071/BT19034
Gonzalez SL, Ghermandi L (2019) Dwarf shrub facilitates seedling recruitment and plant diversity in semiarid grasslands. PLoS One 14:1–17. https://doi.org/10.1371/journal.pone.0212058
Hakimi Y, Fatahi R, Naghavi MR (2021) Seed germination indices of Papaver bracteatum populations under different temperature treatments. Natl Seed Sci Technol Conf Iran 3–10
Hartig F (2019) DHARMa: Residual diagnostics for hierarchical (multi-level / mixed) regression models. R package version 0.2.4. https://CRAN.R-project.org/package=DHARMa. Assessed 24 Aug 2020
Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science (80) 324:636–638 https://doi.org/10.1126/science.1169640
Hendriks M, Mommer L, de Caluwe H et al (2013) Independent variations of plant and soil mixtures reveal soil feedback effects on plant community overyielding. J Ecol 101:287–297. https://doi.org/10.1111/1365-2745.12032
Herrera Paredes S, Lebeis SL (2016) Giving back to the community: microbial mechanisms of plant–soil interactions. Funct Ecol 30:1043–1052. https://doi.org/10.1111/1365-2435.12684
Hogenhout SA, Loria R (2008) Virulence mechanisms of Gram-positive plant pathogenic bacteria. Curr Opin Plant Biol 11:449–456. https://doi.org/10.1016/j.pbi.2008.05.007
Hortal S, Bastida F, Armas C et al (2013) Soil microbial community under a nurse-plant species changes in composition, biomass and activity as the nurse grows. Soil Biol Biochem 64:139–146. https://doi.org/10.1016/j.soilbio.2013.04.018
Hovenden MJ, Wills KE, Chaplin RE et al (2008) Warming and elevated CO2 affect the relationship between seed mass, germinability and seedling growth in Austrodanthonia caespitosa, a dominant Australian grass. Glob Chang Biol 14:1633–1641. https://doi.org/10.1111/j.1365-2486.2008.01597.x
Hoyle GL, Venn SE, Steadman KJ et al (2013) Soil warming increases plant species richness but decreases germination from the alpine soil seed bank. Glob Chang Biol 19:1549–1561. https://doi.org/10.1111/gcb.12135
Huang K, Kardol P, Yan X et al (2021) Plant–soil biota interactions explain shifts in plant community composition under global change. Funct Ecol 35:2778–2788. https://doi.org/10.1111/1365-2435.13940
Huang Z, Footitt S, Tang A, Finch-Savage WE (2018) Predicted global warming scenarios impact on the mother plant to alter seed dormancy and germination behaviour in Arabidopsis. Plant Cell Environ 41:187–197. https://doi.org/10.1111/pce.13082
Jones SE, Ho L, Rees CA et al (2017) Streptomyces exploration is triggered by fungal interactions and volatile signals. Elife 6:1–21. https://doi.org/10.7554/eLife.21738
Ke P, Zee PC, Fukami T (2021) Dynamic plant – soil microbe interactions : the neglected effect of soil conditioning time. New Phytol. https://doi.org/10.1111/nph.17420
Kõljalg U, Larsson KH, Abarenkov K et al (2005) UNITE: A database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068. https://doi.org/10.1111/j.1469-8137.2005.01376.x
Kremer RJ (1993) Management of weed seed banks with microorganisms. Ecol Appl 3:42–52. https://doi.org/10.2307/1941791
Kudernatsch T, Fischer A, Bernhardt-Römermann M, Abs C (2008) Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species. Basic Appl Ecol 9:263–274. https://doi.org/10.1016/j.baae.2007.02.005
Kulmatiski A, Anderson-Smith A, Beard KH et al (2014) Most soil trophic guilds increase plant growth: a meta-analytical review. Oikos 123:1409–1419. https://doi.org/10.1111/oik.01767
Lazarus BE, Castanha C, Germino MJ et al (2018) Growth strategies and threshold responses to water deficit modulate effects of warming on tree seedlings from forest to alpine. J Ecol 106:571–585. https://doi.org/10.1111/1365-2745.12837
Li C, Shimono A, Shen H, Tang Y (2010) Phylogeography of Potentilla fruticosa, an alpine shrub on the Qinghai-Tibetan Plateau. J Plant Ecol 3:9–15. https://doi.org/10.1093/jpe/rtp022
Liu K, Baskin JM, Baskin CC et al (2013) Effect of Diurnal Fluctuating versus Constant Temperatures on Germination of 445 Species from the Eastern Tibet Plateau. PLoS One 8:1–10. https://doi.org/10.1371/journal.pone.0069364
Lozano YM, Armas C, Hortal S et al (2017) Disentangling above- and below-ground facilitation drivers in arid environments: the role of soil microorganisms, soil properties and microhabitat. New Phytol 216:1236–1246. https://doi.org/10.1111/nph.14499
Lozano YM, Hortal S, Armas C, Pugnaire FI (2020) Complementarity in nurse plant systems: soil drives community composition while microclimate enhances productivity and diversity. Plant Soil 450:385–396. https://doi.org/10.1007/s11104-020-04503-6
Luo W, Callaway RM, Atwater DZ (2016) Intraspecific diversity buffers the inhibitory effects of soil biota. Ecology 97:1913–1918. https://doi.org/10.1002/ecy.1469
Magoč T, Salzberg SL (2011) FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Michalet R, Brooker RW, Lortie CJ et al (2015) Disentangling direct and indirect effects of a legume shrub on its understorey community. Oikos 124:1251–1262. https://doi.org/10.1111/oik.01819
Milbau A, Graae BJ, Shevtsova A, Nijs I (2009) Effects of a warmer climate on seed germination in the subarctic. Ann Bot 104:287–296. https://doi.org/10.1093/aob/mcp117
Miller EC, Perron GG, Collins CD (2019) Plant-driven changes in soil microbial communities influence seed germination through negative feedbacks. Ecol Evol 9:9298–9311. https://doi.org/10.1002/ece3.5476
Molau U (1997) Responses to natural climatic variation and experimental warming in two tundra plant species with contrasting life forms: Cassiope tetragona and Ranunculus nivalis. Glob Chang Biol 3:97–107. https://doi.org/10.1111/j.1365-2486.1997.gcb138.x
Molina-Montenegro MA, Oses R, Atala C et al (2016) Nurse effect and soil microorganisms are key to improve the establishment of native plants in a semiarid community. J Arid Environ 126:54–61. https://doi.org/10.1016/j.jaridenv.2015.10.016
Myers-Smith IH, Hik DS (2013) Shrub canopies influence soil temperatures but not nutrient dynamics: An experimental test of tundra snow-shrub interactions. Ecol Evol 3:3683–3700. https://doi.org/10.1002/ece3.710
Nguyen NH, Song Z, Bates ST et al (2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Nuske SJ, Fajardo A, Nu MA et al (2021) Soil biotic and abiotic effects on seedling growth exhibit context- dependent interactions : evidence from a multi-country experiment on Pinus contorta invasion. New Phytol 303–317 https://doi.org/10.1111/nph.17449
Oksanen AJ, Blanchet FG, Friendly M et al (2020) Vegan: community ecology, package. R package version 2.5–6. Journal of Statistical Software 48, 103–132.
Ooi MKJ (2012) Seed bank persistence and climate change. Seed Sci Res 22 https://doi.org/10.1017/S0960258511000407
Parmesan C, Hanley ME (2015) Plants and climate change: Complexities and surprises. Ann Bot 116:849–864. https://doi.org/10.1093/aob/mcv169
Pugnaire FI, Armas C, Valladares F (2004) Soil as a mediator in plant-plant interactions in a semi-arid community. J Veg Sci 15:85–92. https://doi.org/10.1111/j.1654-1103.2004.tb02240.x
Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219
Rasmussen PU, Bennett AE, Tack AJM (2020) The impact of elevated temperature and drought on the ecology and evolution of plant–soil microbe interactions. J Ecol 108:337–352. https://doi.org/10.1111/1365-2745.13292
Reinhart KO, Royo AA, Van Der Putten WH, Clay K (2005) Soil feedback and pathogen activity in Prunus serotina throughout its native range. J Ecol 93:890–898. https://doi.org/10.1111/j.1365-2745.2005.01028.x
R Core Team. 2020 “R: A Language and environment for statistical computing and graphics.” http://www.R-project.org/. Accessed 17 Apr 2020
Rixen C, Mulder CPH (2009) Species removal and experimental warming in a subarctic tundra plant community. Oecologia 161:173–186. https://doi.org/10.1007/s00442-009-1369-y
Rodríguez-Echeverría S, Lozano YM, Bardgett RD (2016) Influence of soil microbiota in nurse plant systems. Funct Ecol 30:30–40. https://doi.org/10.1111/1365-2435.12594
Schöb C, Armas C, Pugnaire FI (2013) Direct and indirect interactions co-determine species composition in nurse plant systems. Oikos 122:1371–1379. https://doi.org/10.1111/j.1600-0706.2013.00390.x
Shi FS, Wu Y, Wu N, Luo P (2010) Different growth and physiological responses to experimental warming of two dominant plant species Elymus nutans and Potentilla anserina in an alpine meadow of the eastern Tibetan Plateau. Photosynthetica 48:437–445. https://doi.org/10.1007/s11099-010-0058-8
Strous M, Jhon AF, Evelien HMK et al (1999) Missing lithotroph identified as new planctomycete. Nature 400:446–449
Tang L, Zhong L, Xue K et al (2019) Warming counteracts grazing effects on the functional structure of the soil microbial community in a Tibetan grassland. Soil Biol Biochem 134:113–121. https://doi.org/10.1016/j.soilbio.2019.02.018
Tian K, Huang B, Xing Z, Hu W (2017) Geochemical baseline establishment and ecological risk evaluation of heavy metals in greenhouse soils from Dongtai, China. Ecol Indic 72:510–520. https://doi.org/10.1016/j.ecolind.2016.08.037
Van der Putten WH, Bardgett RD, Bever JD et al (2013) Plant-soil feedbacks: The past, the present and future challenges. J Ecol 101:265–276. https://doi.org/10.1111/1365-2745.12054
Wickham H (2008) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York
Winkler DE, Lubetkin KC, Carrell AA et al (2019) Responses of alpine plant communities to climate warming. Ecosyst Consequences Soil Warm Microbes, Veg Fauna Soil Biogeochem. Academic Press, Cambridge, pp 297–346
Xu J, Michalet R, Zhang JL et al (2010) Assessing facilitative responses to a nurse shrub at the community level: The example of Potentilla fruticosa in a sub-alpine grassland of northwest China. Plant Biol 12:780–787. https://doi.org/10.1111/j.1438-8677.2009.00271.x
Zhao D, Zhu Y, Wu S, Zheng D (2021) Projection of vegetation distribution to 1.5 °C and 2 °C of global warming on the Tibetan Plateau. Glob Planet Change 20a2:103525 https://doi.org/10.1016/j.gloplacha.2021.103525
Zhou H, Yue H, Ai X et al (2015) Poor seed dispersal, seed germination and seedling survival explain why rubber trees (Hevea brasiliensis) do not expand into natural forests in Xishuangbanna, southwest China. For Ecol Manage 358:240–247. https://doi.org/10.1016/j.foreco.2015.09.023
Zhou Z, Liu Y, Zhu Q, et al (2020) Comparing the variations and controlling factors of soil N2O emissions and NO3–-N leaching on tea and bamboo hillslopes. Catena 188:104463 https://doi.org/10.1016/j.catena.2020.104463
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This work was funded from the Project of the National Natural Science Foundation of China (41830321, 31870412, 31670435, 31670437), the “111 Project” (BP0719040), and supported from the Gansu Gannan Grassland Ecosystem National Observation and Research Station.
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Kun Liu and Ziyang Liu. designed the experiments; Shuyan Chen, Xiangtai Wang, Lizhe An, Jinwei Chen, Hanwen Cui, Hongxian Song, Xiaoli Yang, Lihua Meng, Haining Gao, Jiajia Wang and Yajun Wang collected field and laboratorial data. Jiajia Wang and Sa Xiao performed statistical analysis and made the figures. Jiajia Wang, Stephen Patrick Bonser and Sa Xiao drafted the manuscript. All authors contributed to the manuscript.
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Wang, J., Bonser, S.P., Liu, K. et al. Warming affects herbaceous germination, early survival, and growth by shifting plant-soil microbe interactions in an alpine ecosystem. Plant Soil 487, 249–265 (2023). https://doi.org/10.1007/s11104-023-05921-y
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DOI: https://doi.org/10.1007/s11104-023-05921-y