Rhizosphere microbe populations but not root traits induced by drought in Populus euphratica males

Zhichao Xia, Yue He, Jiahui Xu, Zuodong Zhu, Helena Korpelainen, Chunyang Li

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Soil Ecology Letters ›› 2023, Vol. 5 ›› Issue (2) : 220152. DOI: 10.1007/s42832-022-0152-4
RESEARCH ARTICLE

Rhizosphere microbe populations but not root traits induced by drought in Populus euphratica males

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Highlights

● Sexually dimorphic belowground responses to cope with drought.

● Females show more morphological plasticity in response to water deficiency.

● Males influence rhizosphere micro-organisms to compensate for resource acquisition.

● Microbial responses are associated with root trait adjustments to drought.

Abstract

How sex-related root traits and soil microbes and their interactions respond to drought remains unclear. Here, we investigated how fine root traits and the composition of rhizosphere microbial communities in Populus euphratica females and males respond to drought in concert in 17-year-old plantations. Females increased specific root length (SRL) in response to drought. However, males showed no changes in their roots but significant increases in arbuscular mycorrhizal hyphal biomass and population of Gram-negative bacteria in the rhizosphere. Also, fungal symbiotroph communities associated with root systems in males differed from those in females under drought. We further demonstrated that the Gram-positive to Gram-negative bacteria ratios positively correlated with the SRL, while fungi to bacteria ratios were negatively correlated. Meanwhile, the relative abundance of symbiotrophs was negatively correlated with the SRL, while saprotroph abundance was positively correlated. Nevertheless, the relative abundance of symbiotrophs was positively correlated with the root carbon content (RCC). These findings indicate that microbial responses to drought depend highly upon the sex of the plant and microbial group and are related to root trait adjustments to drought. This discovery also highlights the role of plant-microbial interactions in the ecosystems of P. euphratica forest plantations.

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Keywords

Dioecy / Drought / Root functional traits / Root-soil-microbe interactions / Fungal functional guilds / Sex-specific responses

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Zhichao Xia, Yue He, Jiahui Xu, Zuodong Zhu, Helena Korpelainen, Chunyang Li. Rhizosphere microbe populations but not root traits induced by drought in Populus euphratica males. Soil Ecology Letters, 2023, 5(2): 220152 https://doi.org/10.1007/s42832-022-0152-4

References

[1]
Balachowski, J.A., Volaire, F.A., 2018. Implications of plant functional traits and drought survival strategies for ecological restoration. Journal of Applied Ecology55, 631–640.
CrossRef Google scholar
[2]
Bhusal, N., Lee, M., Lee, H., Adhikari, A., Han, A.R., Han, A., Kim, H.S., 2021. Evaluation of morphological, physiological, and biochemical traits for assessing drought resistance in eleven tree species. Science of the Total Environment779, 146466.
CrossRef Google scholar
[3]
Broeckling, C.D., Broz, A.K., Bergelson, J., Manter, D.K., Vivanco, J.M., 2008. Root exudates regulate soil fungal community composition and diversity. Applied and Environmental Microbiology74, 738–744.
CrossRef Google scholar
[4]
Brundrett, M.C., 2002. Coevolution of roots and mycorrhizas of land plants. New Phytologist154, 275–304.
CrossRef Google scholar
[5]
Brunner, I., Herzog, C., Dawes, M.A., Arend, M., Sperisen, C., 2015. How tree roots respond to drought. Frontiers in Plant Science6, 547.
CrossRef Google scholar
[6]
de Vries, F.T., Griffiths, R.I., Knight, C.G., Nicolitch, O., Williams, A., 2020. Harnessing rhizosphere microbiomes for drought-resilient crop production. Science368, 270–274.
CrossRef Google scholar
[7]
Debinski, D.M., Wickham, H., Kindscher, K., Caruthers, J.C., Germino, M., 2010. Montane meadow change during drought varies with background hydrologic regime and plant functional group. Ecology91, 1672–1681.
CrossRef Google scholar
[8]
Doniger, T., Adams, J.M., Marais, E., Maggs-Kölling, G., Sherman, C., Kerfahi, D., Yang, Y., Steinberger, Y., 2020. The ‘fertile island effect’ of Welwitschia plants on soil microbiota is influenced by plant gender. FEMS Microbiology Ecology96, fiaa186.
CrossRef Google scholar
[9]
Fanin, N., Kardol, P., Farrell, M., Nilsson, M.C., Gundale, M.J., Wardle, D.A., 2019. The ratio of Gram-positive to Gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils. Soil Biology & Biochemistry128, 111–114.
CrossRef Google scholar
[10]
Freschet, G.T., Pagès, L., Iversen, C.M., Comas, L.H., Rewald, B., Roumet, C., Klimešová, J., Zadworny, M., Poorter, H., Postma, J.A., Adams, T.S., Bagniewska-Zadworna, A., Bengough, A.G., Blancaflor, E.B., Brunner, I., Cornelissen, J.H.C., Garnier, E., Gessler, A., Hobbie, S.E., Meier, I.C., Mommer, L., Picon-Cochard, C., Rose, L., Ryser, P., Scherer-Lorenzen, M., Soudzilovskaia, N.A., Stokes, A., Sun, T., Valverde-Barrantes, O.J., Weemstra, M., Weigelt, A., Wurzburger, N., York, L.M., Batterman, S.A., Gomes de Moraes, M., Janeček, Š., Lambers, H., Salmon, V., Tharayil, N., McCormack, M.L., 2021a. A starting guide to root ecology: strengthening ecological concepts and standardizing root classification, sampling, processing and trait measurements. New Phytologist232, 973–1122.
CrossRef Google scholar
[11]
Freschet, G.T., Roumet, C., Comas, L.H., Weemstra, M., Bengough, A.G., Rewald, B., Bardgett, R.D., De Deyn, G.B., Johnson, D., Klimešová, J., Lukac, M., McCormack, M.L., Meier, I.C., Pagès, L., Poorter, H., Prieto, I., Wurzburger, N., Zadworny, M., Bagniewska-Zadworna, A., Blancaflor, E.B., Brunner, I., Gessler, A., Hobbie, S.E., Iversen, C.M., Mommer, L., Picon-Cochard, C., Postma, J.A., Rose, L., Ryser, P., Scherer-Lorenzen, M., Soudzilovskaia, N.A., Sun, T., Valverde-Barrantes, O.J., Weigelt, A., York, L.M., Stokes, A., 2021b. Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs. New Phytologist232, 1123–1158.
CrossRef Google scholar
[12]
Goebel, M., Hobbie, S.E., Bulaj, B., Zadworny, M., Archibald, D.D., Oleksyn, J., Reich, P.B., Eissenstat, D.M., 2011. Decomposition of the finest root branching orders: linking belowground dynamics to fine-root function and structure. Ecological Monographs81, 89–102.
CrossRef Google scholar
[13]
Guo, Q., Liu, J., Yu, L., Korpelainen, H., Li, C., 2021. Different sexual impacts of dioecious Populus euphratica on microbial communities and nitrogen cycle processes in natural forests. Forest Ecology and Management496, 119403.
CrossRef Google scholar
[14]
Huang, X., Liu, S., Liu, X., Zhang, S., Li, L., Zhao, H., Zhao, J., Zhang, J., Cai, Z., 2020. Plant pathological condition is associated with fungal community succession triggered by root exudates in the plant-soil system. Soil Biology & Biochemistry151, 108046.
CrossRef Google scholar
[15]
Hultine, K.R., Grady, K.C., Wood, T.E., Shuster, S.M., Stella, J.C., Whitham, T.G., 2016. Climate change perils for dioecious plant species. Nature Plants2, 16109.
CrossRef Google scholar
[16]
Juvany, M., Munne-Bosch, S., 2015. Sex-related differences in stress tolerance in dioecious plants: a critical appraisal in a physiological context. Journal of Experimental Botany66, 6083–6092.
CrossRef Google scholar
[17]
Kannenberg, S.A., Phillips, R.P., 2017. Soil microbial communities buffer physiological responses to drought stress in three hardwood species. Oecologia183, 631–641.
CrossRef Google scholar
[18]
Laliberté, E., Lambers, H., Burgess, T.I., Wright, S.J., 2015. Phosphorus limitation, soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrub lands. New Phytologist206, 507–521.
CrossRef Google scholar
[19]
Lei, Y., Jiang, Y., Chen, K., Duan, B., Zhang, S., Korpelainen, H., Niinemets, U., Li, C., 2017. Reproductive investments driven by sex and altitude in sympatric Populus and Salix trees. Tree Physiology37, 1503–1514.
CrossRef Google scholar
[20]
Lin, G., McCormack, M.L., Guo, D., 2015. Arbuscular mycorrhizal fungal effects on plant competition and community structure. Journal of Ecology103, 1224–1232.
CrossRef Google scholar
[21]
Liu, B., Li, H., Zhu, B., Koide, R.T., Eissenstat, D.M., Guo, D., 2015. Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytologist208, 125–136.
CrossRef Google scholar
[22]
Liu, J., Feng, H., He, J., Chen, H., Ding, D., 2018. The effects of nitrogen and water stresses on the nitrogen-to-protein conversion factor of winter wheat. Agricultural Water Management210, 217–223.
CrossRef Google scholar
[23]
Liu, J., Zhang, R., Xu, X., Fowler, J.C., Miller, T.E., Dong, T., 2020. Effect of summer warming on growth, photosynthesis and water status in female and male Populus cathayana: implications for sex-specific drought and heat tolerances. Tree Physiology40, 1178–1191.
CrossRef Google scholar
[24]
Liu, M., Korpelainen, H., Li, C., 2021a. Sexual differences and sex ratios of dioecious plants under stressful environments. Journal of Plant Ecology14, 920–933.
CrossRef Google scholar
[25]
Liu, M., Wang, Y., Liu, X., Korpelainen, H., Li, C., 2021b. Intra- and intersexual interactions shape microbial community dynamics in the rhizosphere of Populus cathayana females and males exposed to excess Zn. Journal of Hazardous Materials402, 123783.
CrossRef Google scholar
[26]
Lozano, Y.M., Aguilar-Trigueros, C.A., Roy, J., Rillig, M.C., 2021. Drought induces shifts in soil fungal communities that can be linked to root traits across twenty-four plant species. New Phytologist232, 1917–1929.
CrossRef Google scholar
[27]
Mangiafico, S., Mangiafico, M.S., 2017. Package ‘rcompanion’. Cran Repos20, 1–71.
[28]
Melnikova, N.V., Borkhert, E.V., Snezhkina, A.V., Kudryavtseva, A.V., Dmitriev, A.A., 2017. Sex-specific response to stress in Populus. Frontiers in Plant Science8, 6.
CrossRef Google scholar
[29]
Naylor, D., Coleman-Derr, D., 2018. Drought stress and root-associated bacterial communities. Frontiers in Plant Science8, 2223.
CrossRef Google scholar
[30]
Nguyen, N.H., Song, Z., Bates, S.T., Branco, S., Tedersoo, L., Menke, J., Schilling, J.S., Kennedy, P.G., 2016. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology20, 241–248.
CrossRef Google scholar
[31]
Nikolova, P.S., Bauerle, T.L., Häberle, K.H., Blaschke, H., Brunner, I., Matyssek, R., 2020. Fine-root traits reveal contrasting ecological strategies in European beech and Norway spruce during extreme drought. Frontiers in Plant Science11, 1211.
CrossRef Google scholar
[32]
Nowak, K., Giertych, M.J., Pers-Kamczyc, E., Thomas, P.A., Iszkuło, G., 2021. Rich but not poor conditions determine sex-specific differences in growth rate of juvenile dioecious plants. Journal of Plant Research134, 947–962.
CrossRef Google scholar
[33]
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P., O’Hara, R., Simpson, G., Solymos, P., Henry, M., Stevens, M., 2015. Vegan community ecology package: ordination methods, diversity analysis and other functions for community and vegetation ecologists. R package ver, 2–3.
[34]
Olmo, M., Lopez-Iglesias, B., Villar, R., 2014. Drought changes the structure and elemental composition of very fine roots in seedlings of ten woody tree species. Implications for a drier climate. Plant and Soil384, 113–129.
CrossRef Google scholar
[35]
Orwin, K.H., Dickie, I., Holdaway, R., Wood, J., 2018. A comparison of the ability of PLFA and 16S rRNA gene metabarcoding to resolve soil community change and predict ecosystem functions. Soil Biology & Biochemistry117, 27–35.
CrossRef Google scholar
[36]
Randriamanana, T.R., Nybakken, L., Lavola, A., Aphalo, P.J., Nissinen, K., Julkunen-Tiitto, R., 2014. Sex-related differences in growth and carbon allocation to defence in Populus tremula as explained by current plant defence theories. Tree Physiology34, 471–487.
CrossRef Google scholar
[37]
Renner, S.S., 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany101, 1588–1596.
CrossRef Google scholar
[38]
Retuerto, R., Vilas, J.S., Varga, S., 2018. Sexual dimorphism in response to stress. Environmental and Experimental Botany146, 1–4.
CrossRef Google scholar
[39]
Revelle, W., 2017. Procedures for personality and psychological research. Northwestern University, Evanston, Illinois, USA
[40]
Schimel, J.P., 2018. Life in dry soils: effects of drought on soil microbial communities and processes. Annual Review of Ecology, Evolution, and Systematics49, 409–432.
CrossRef Google scholar
[41]
Semchenko, M., Leff, J.W., Lozano, Y.M., Saar, S., Davison, J., Wilkinson, A., Jackson, B.G., Pritchard, W.J., Jonathan, R., Oakley, S., 2018. Fungal diversity regulates plant-soil feedbacks in temperate grassland. Science Advances4, eaau4578.
CrossRef Google scholar
[42]
Simpson, G., 2015. ggvegan: ‘ggplot2’ Plots for the ‘vegan’ Package. R package version00–3.
[43]
Spitzer, C.M., Lindahl, B., Wardle, D.A., Sundqvist, M.K., Gundale, M.J., Fanin, N., Kardol, P., 2021. Root trait–microbial relationships across tundra plant species. New Phytologist229, 1508–1520.
CrossRef Google scholar
[44]
Sweeney, C.J., de Vries, F.T., van Dongen, B.E., Bardgett, R.D., 2021. Root traits explain rhizosphere fungal community composition among temperate grassland plant species. New Phytologist229, 1492–1507.
CrossRef Google scholar
[45]
Tang, S., Liang, H., Yan, D., Zhao, Y., Han, X., Carlson, J.E., Xia, X., Yin, W., 2013. Populus euphratica: the transcriptomic response to drought stress. Plant Molecular Biology83, 539–557.
CrossRef Google scholar
[46]
Vu, V.Q., 2016. Ggbiplot: A ggplot2 based biplot. R package version 0.55. 2011
[47]
Wan, X., Chen, X., Huang, Z., Chen, H.Y., 2021. Contribution of root traits to variations in soil microbial biomass and community composition. Plant and Soil460, 483–495.
CrossRef Google scholar
[48]
Wickham, H., 2016. ggplot2-Elegant Graphics for Data Analysis. Springer International Publishing. Cham, Switzerland
[49]
Wu, X., Liu, J., Meng, Q., Fang, S., Kang, J., Guo, Q., 2021. Differences in carbon and nitrogen metabolism between male and female Populus cathayana in response to deficient nitrogen. Tree Physiology41, 119–133.
CrossRef Google scholar
[50]
Xia, M., Valverde‐Barrantes, O.J., Suseela, V., Blackwood, C.B., Tharayil, N., 2021a. Coordination between compound-specific chemistry and morphology in plant roots aligns with ancestral mycorrhizal association in woody angiosperms. New Phytologist232, 1259–1271.
CrossRef Google scholar
[51]
Xia, Z., He, Y., Korpelainen, H., Niinemets, Ü., Li, C., 2022. Sex-specific interactions shape root phenolics and rhizosphere microbial communities in Populus cathayana. Forest Ecology and Management504, 119857.
CrossRef Google scholar
[52]
Xia, Z., He, Y., Yu, L., Li, Z., Korpelainen, H., Li, C., 2021b. Revealing interactions between root phenolic metabolomes and rhizosphere bacterial communities in Populus euphratica plantations. Biology and Fertility of Soils57, 421–434.
CrossRef Google scholar
[53]
Xia, Z., He, Y., Yu, L., Lv, R., Korpelainen, H., Li, C., 2020a. Sex-specific strategies of phosphorus (P) acquisition in Populus cathayana as affected by soil P availability and distribution. New Phytologist225, 782–792.
CrossRef Google scholar
[54]
Xia, Z., He, Y., Zhou, B., Korpelainen, H., Li, C., 2020b. Sex-related responses in rhizosphere processes of dioecious Populus cathayana exposed to drought and low phosphorus stress. Environmental and Experimental Botany175, 104049.
CrossRef Google scholar
[55]
Xia, Z., Yu, L., He, Y., Korpelainen, H., Li, C., 2019. Broadleaf trees mediate chemically the growth of Chinese fir through root exudates. Biology and Fertility of Soils55, 737–749.
CrossRef Google scholar
[56]
Xu, X., Peng, G., Wu, C., Korpelainen, H., Li, C., 2008a. Drought inhibits photosynthetic capacity more in females than in males of Populus cathayana. Tree Physiology28, 1751–1759.
CrossRef Google scholar
[57]
Xu, X., Yang, F., Xiao, X., Zhang, S., Korpelainen, H., Li, C., 2008b. Sex-specific responses of Populus cathayana to drought and elevated temperatures. Plant, Cell & Environment31, 850–860.
CrossRef Google scholar
[58]
Yu, L., Dong, H., Li, Z., Han, Z., Korpelainen, H., Li, C., 2020. Species-specific responses to drought, salinity and their interactions in Populus euphratica and P. pruinosa seedlings. Journal of Plant Ecology13, 563–573.
CrossRef Google scholar
[59]
Zhang, Y., Xu, G., Peng, S., Bai, J., Lu, Q., Duan, B., 2021. Water relations and non-structural carbohydrate responses to the combined effects of defoliation and progressive drought in a dioecious tree. New Forests52, 605–619.
CrossRef Google scholar
[60]
Zufferey, V., Cochard, H., Ameglio, T., Spring, J.L., Viret, O., 2011. Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas). Journal of Experimental Botany62, 3885–3894.
CrossRef Google scholar

Conflict of interest

The authors declare that they have no conflict of interest.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. U1803231).

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Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-022-0152-4 and is accessible for authorized users.

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