根际微生物介导的植物响应干旱胁迫机制研究进展

曹亚静; 赵美丞; 郑春燕; 朱峰

doi:10.12357/cjea.20230127

根际微生物介导的植物响应干旱胁迫机制研究进展

doi: 10.12357/cjea.20230127

曹亚静^{1, 2,},
赵美丞¹,
郑春燕¹,
朱峰^1, ,

1.
河北省土壤生态学重点实验室/中国科学院农业水资源重点实验室/中国科学院遗传与发育生物学研究所农业资源研究中心　石家庄　050022
2.
中国科学院大学　北京　100049

基金项目: 国家重点研发青年科学家项目(2021YFD1900200)、中国科院科技服务网络(STS)计划(KFJ-STS-QYZD-160)、国家重点研发计划项目(2022YFF1302801)和中国科学院“百人计划”资助

详细信息

作者简介:
曹亚静, 主要从事植物介导地上地下互作机制研究。E-mail: caoyajing20@mails.ucas.ac.cn

通讯作者:
朱峰, 主要从事植物介导地上地下互作机制研究。E-mail: zhufeng@sjziam.ac.cn

中图分类号: S154.36
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出版历程
- 收稿日期: 2023-03-10
- 录用日期: 2023-04-06
- 修回日期: 2023-05-05
- 网络出版日期: 2023-05-23

Rhizosphere microorganisms-mediated plant responses to drought stress

CAO Yajing^{1, 2
,},
ZHAO Meicheng¹,
ZHENG Chunyan¹,
ZHU Feng^{1
, ,}

1.
Hebei Key Laboratory of Soil Ecology / Key Laboratory of Agricultural Water Resources / Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang 050022, China
2.
University of Chinese Academy of Sciences, Beijing 100049, China

Funds: This study was supported by the Young Scientists Project of National Key Research and Development Program of China (2021YFD1900200), the Science and Technology Service Network Initiative of Chinese Academy of Sciences (KFJ-STS-QYZD-160), the National Key Research and Development Program of China (2022YFF1302801) and the ‘100 Talents Project’ of Chinese Academy of Sciences.

More Information

Corresponding author: E-mail: zhufeng@sjziam.ac.cn

摘要

摘要: 干旱作为目前全球农业生产面临的自然灾害之一, 严重制约着粮食安全和农业可持续发展。仅仅依赖于植物自身应对干旱的生理响应开发作物抗旱策略是远远不够的。关注干旱胁迫下适应性微生物的定殖以及微生物对植物的有益协助, 对改善植物生长并提高作物抗旱能力具有重要的指导意义。其中, 与植物紧密互作的根际微生物在植物健康发育和胁迫耐受性方面发挥着重要作用, 具备良好的应用潜力。本文总结了干旱胁迫对植物根际微生物群落多样性及组成的影响, 发现放线菌、厚壁菌以及丛枝菌根真菌在干旱下出现明显富集; 剖析了根际相关微生物协助植物抵御干旱胁迫的机制, 包括分泌植物生长调节因子、合成ACC脱氨酶、产生胞外多糖以及增强植物抗氧化酶活性等方式, 以期挖掘与植物高抗旱能力相关的潜在微生物并充分发挥其作用。最后, 本文提出未来不仅应该加大对植物耐旱野生近缘种的开发利用, 探寻与之存在有益协作关系的微生物来源并加以恢复, 还应从管理和调控植物微生物组的角度充分发挥植物根际微生物组在增强作物抗旱性中的作用, 为全球气候变暖背景下的可持续农业应用提供新思路。
- 干旱胁迫 /
- 根际微生物 /
- 根际促生细菌 /
- 根际促生真菌 /
- 丛枝菌根真菌
Abstract: As one of the consequences of climate change, drought has been seriously restricting global food security and the sustainable development of agriculture. Developing crop drought resistance not only rely on diverse genetic resources, but it is also important to explore the colonizing adaptive microorganisms as well as the potential beneficial associations between plants and microbes under drought condition. Among them, rhizosphere microorganisms that interact closely with plants play important roles in plant growth and stress tolerance. In this paper, we first discuss the effects of drought stress on the diversity and composition of plant rhizosphere microbial communities. In the rhizosphere compartment, Actinobacteria, Firmicutes and arbuscular mycorrhiza fungi are often significantly enriched under drought stress. Next, we also address the mechanisms of rhizosphere microorganisms assisting plants to resist drought stress, especially how rhizosphere microorganisms regulate plant stress responses, including the secretion of plant growth regulators, the synthesis of ACC deaminase, the production of exopolysaccharides and the enhancement of plant antioxidant enzyme activity, etc. Finally, we suggest that exploring drought-tolerant wild relatives and their associated beneficial microbes may further help microbiome-assisted plant breeding programs. In addition, the construction and application of synthetic communities of beneficial rhizosphere microbiomes may improve drought resistance and sustainable production of crops in the context of global environmental changes.
- Drought stress /
- Rhizosphere microorganisms /
- Plant growth promoting bacteria /
- Plant growth promoting fungi /
- Arbuscular mycorrhiza fungi

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图 1 根际微生物介导植物响应干旱胁迫的模式图型

ROS: 活性氧; ABA: 脱落酸; “↑”表示升高; “↓”表示降低。ROS: reactive oxygen species; ABA: abscisic acid; “↑”indicates increase; “↓”indicates reduction.

Figure 1. A diagram of plant response to drought stress mediated by rhizosphere microorganisms

下载: 全尺寸图片幻灯片

图 2 根际微生物介导植物抗旱机制模式图

PGPB: 植物根际促生细菌; PGPF: 植物根际促生真菌; AMF: 丛枝菌根真菌; Protozoa: 原生动物; Microalgae: 微藻; AM: 丛枝菌根; IAA: 吲哚-3-乙酸; ABA: 脱落酸; CTK: 细胞分裂素; GA: 赤霉素; ACC: 1-氨基环丙烷-1-羧酸; EPS: 胞外多糖; POD: 过氧化物酶; SOD: 超氧化物歧化酶; CAT: 过氧化氢酶。PGPB: plant growth promoting bacteria; PGPF: plant growth promoting fungi; AMF: arbuscular mycorrhiza fungi; AM: arbuscular mycorrhiza; IAA: indole-3-acetic acid; ABA: abscisic acid; CTK: cytokinin; GA: gibberellic acid; ACC: 1-aminocyclopropane-1-carboxylic acid; EPS: exopoly saccharides; POD: peroxidase; SOD: superoxide dismutase; CAT: catalase.

Figure 2. Pattern diagram of plant drought resistance mechanism mediated by rhizosphere associated microorganisms

下载: 全尺寸图片幻灯片

表 1 根际促生细菌(PGPB)对植物响应干旱胁迫的影响及作用机制

Table 1. Effect and functional mechanism of plant growth promoting bacteria (PGPB) rhizosphere soil on plant response to drought stress

细菌属 Bacteria genus	细菌种 Bacteria species	植物种 Plant species	影响及作用机制 Effect and functional mechanism	文献 Reference
芽孢杆菌属 Bacillus	苏云金芽孢杆菌 B. thuringiensis	薰衣草 Lavandula angustifolia	产生IAA, 增加钾含量、积累脯氨酸 Produce IAA, increase potassium content and accumulate proline	[49]
	枯草芽孢杆菌LDR2 B. subtilis	小麦 Triticum aestivum	产生IAA, 提高光合速率 Produce IAA and improve photosynthetic rate	[50]
	地衣芽孢杆菌K11 B. licheniformis	辣椒 Capsicum annuum	产生IAA, 增加植株根长、茎长和干重 Produce IAA, increase plant root length, stem length and dry weight	[51]
	枯草芽孢杆菌 B. subtilis	侧柏 Platycladus orientalis	产生ABA, 增加叶片含水量 Produce ABA and increase leaf water content	[53]
	短小芽孢杆菌 B. pumilus	甘草 Glycyrrhiza uralensis	增强抗氧化酶活性, 促进类胡萝卜素和类黄酮代谢 Enhance antioxidant enzyme activity and promote carotenoid and flavonoid metabolism	[62]
	芽孢杆菌 Bacillus sp.	水稻 Oryza sativa	增加抗氧化酶活性, 增加根干重和脯氨酸积累 Increase antioxidant enzyme activity, increase root dry weight and proline accumulation	[64]
	枯草芽孢杆菌 B. subtilis	鹰嘴豆 Cicer arietinum	产EPS, 增加叶面积、根长、根面积 Produce EPS, increase leaf area, root length and root area	[71]
假单胞菌属 Pseudomonas	铜绿假单胞菌 P. aeruginosa	绿豆 Vigna radiata	产生IAA, 茎长、光合活性和抗氧化性能均有显著提高 IAA production, stem length, photosynthetic activity and antioxidant capacity were significantly improved	[52]
	恶臭假单胞菌GAP-P45 P. putida	向日葵 Helianthus annuus	产EPS, 根表面形成生物膜、改善土壤结构 Produce EPS, form biofilm on root surface and improve soil structure	[69]
	恶臭假单胞菌 P. putida	玉米 Zea mays	产EPS, 增加根芽生长、生物量, 改善气孔导度 Produce EPS, increase root and bud growth, biomass, and improve stomatal conductance	[70]
	荧光假单胞菌G型 P. fluorescens	豌豆 Pisum sativum	产ACC脱氨酶, 诱导更长的根系 Produce ACC, induce longer roots	[57]
	假单胞菌 Pseudomonas spp.	豌豆 Pisum sativum	产ACC脱氨酶, 消除对生长、产量和成熟的影响 Produce ACC, eliminate the impact on growth, yield and maturity	[59]
	假单胞菌RRCI5 Pseudomonas sp.	小麦 Triticum aestivum	产ACC脱氨酶, 改善小麦养分状况 Produce ACC, Improve the nutrient status of wheat	[60]
固氮螺菌属 Azospirillum	巴西固氮螺菌 A. brasilense	番茄 Solanum lycopersicum	产生IAA(产生NO信号分子诱导) Production of IAA (induced by production of NO signal molecules)	[48]
	固氮螺菌 Azospirillum sp.	小麦 Triticum aestivum	产生IAA, 增加叶片含水量, 促进根系生长和侧根形成 Produce IAA, increase water content of leaves, promote root growth and lateral root formation	[57]
	生脂固氮螺菌 A. lipoferum	玉米 Zea mays	产生ABA和赤霉素 Produce ABA and gibberellin	[54]
慢生型根瘤菌属Rhizobium	根瘤菌 Rhizobia	小麦 Triticum aestivum	产ACC脱氨酶, 降低根部乙烯浓度, 促进侧根数增加 Produce ACC deaminase, reduce the concentration of ethylene in roots, and promote the increase of lateral roots	[56]
慢生型根瘤菌属Rhizobium	根瘤菌LR-30 Rhizobium leguminosarum	小麦 Triticum aestivum	产EPS, 提高小麦生长、生物量和耐旱指数 Produce EPS, improve wheat growth, biomass and drought tolerance index	[68]
IAA: 吲哚-3-乙酸; ABA: 脱落酸; EPS: 胞外多糖; ACC: 1-氨基环丙烷-1-羧酸。IAA: indole-3-acetic acid; ABA: abscisic acid; EPS: exopoly saccharides; ACC: 1-aminocyclopropane-1-carboxylic acid.

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表 2 根际促生真菌[PGPF, 包括丛枝菌根真菌(AMF)]对植物响应干旱胁迫的影响及作用机制

Table 2. Effect and functional mechanism of plant growth promoting fungi (PGPF) including arbuscular mycorrhiza fungi (AMF) in rhizosphere soil on plant response to drought stress

真菌属 Fungus genus	真菌种 Fungus species	植物种 Plant species	影响及作用机制 Effect and functional mechanism	文献 Reference
曲霉属 Aspergillus	曲霉菌NPF7 Aspergillus sp.	小麦 Triticum aestivum	产生IAA、赤霉素等, 增加植株生长, 提高发芽指数及根系长度 Produce IAA and gibberellin to increase plant growth and improve germination index and root length	[75]
曲霉属 Aspergillus	曲霉菌PPA1 Aspergillus spp.	黄瓜 Cucumis sativus	产生IAA, 增加地上、根部长度及生物量、叶面积和叶绿素含量 Produce IAA, increase aboveground and root length and biomass, leaf area and chlorophyll content	[76]
青霉属 Penicillium	紫青霉菌 P. purpureogenus	水稻 Oryza sativa	增强抗氧化酶活性, 积累可溶性糖及脯氨酸, 增大根长 Enhance antioxidant enzymes activities, accumulate soluble sugar and proline, and increase root length	[77]
木霉属 Trichoderma	深绿木霉 T. atroviride	玉米 Zea mays	增强抗氧化机制 Enhance antioxidant mechanism	[78]
	哈茨木霉 T. harzianum	烟草 Nicotiana tabacum	增强抗氧化酶活性, 增加叶片相对含水量, 降低蒸腾速率 Enhance antioxidant enzymes activities, increase leaf relative water content, and reduce transpiration rate	[79]
	哈茨木霉35 T. harzianum	玉米 Zea mays	增强抗氧化酶活性, 更高的地上部和根干重 Enhanced antioxidant enzyme activity, increase shoot and root dry weight	[74]
茎点霉属 Phoma	茎点霉菌GS8-3 Phoma sp.	烟草 Nicotiana tabacum	产生的2-甲基丙醇和3-甲基丁醇等挥发性混合物促进植株生长 Producted volatile compounds such as 2-methylpropanol and 3-methylbutanol to promote plant growth	[80]
球囊霉属 Glomus (AMF)	地表球囊霉 G. versiforme	玉米 Zea mays	上调抗氧化系统, 维持氧化还原稳态, 消除活性氧 Up-regulate antioxidant system, maintain oxidation-reduction homeostasis and eliminate active oxygen	[85]
	地表球囊霉 G. versiforme	柑橘 Citrus reticulata	增强过氧化物酶活性, 保持土壤水分 Enhance POD activity and maintain soil moisture	[86]
	摩西球囊霉 G. mosseae	柑橘 Citrus reticulata	增强过氧化物酶活性, 保持土壤水分 Enhance POD activity and maintain soil moisture	[86]
	透光球囊霉 G. diaphanum	柑橘 Citrus reticulata	增强过氧化物酶活性, 保持土壤水分 Enhance POD activity and maintain soil moisture	[86]
IAA: 吲哚-3-乙酸; POD: 过氧化物酶。IAA: indole-3-acetic acid; POD: peroxidase.

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参考文献(98)

[1]	BATES B, KUNDZEWICZ Z W, WU S, et al. Climate Change and Water. Technical Paper of the Intergovernmental Panel on Climate Change[M]. Geneva: Climate Change and Water, 2008.
[2]	郑国光. 科学应对全球变暖提高粮食安全保障能力[EB/OL]. 中国气象局, (2009-12-01) [2022-10-21]. http://www.gov.cn/gzdt/2009-12/01/content_1477574.htm ZHENG G G. Scientific response to global warming and improvement of food security capacity[EB/OL]. China Meteorological Administration, (2009-12-01) [2022-10-21]. http://www.gov.cn/gzdt/2009-12/01/content_1477574.htm
[3]	CHAKRABORTY S, NEWTON A C. Climate change, plant diseases and food security: an overview[J]. Plant Pathology, 2011, 60(1): 2−14 doi: 10.1111/j.1365-3059.2010.02411.x
[4]	SELEIMAN M F, AL-SUHAIBANI N, ALI N, et al. Drought stress impacts on plants and different approaches to alleviate its adverse effects[J]. Plants (Basel, Switzerland), 2021, 10(2): 259
[5]	KREEB K, RICHTER H, HINCKLEY T. Structural and functional responses to environmental stresses: water shortage[C]// XIV International Botanical Congress. Structural & Functional Responses to Environmental Stresses: Water Shortage. Hague: SPB Academic Publishing, 1989: 308.
[6]	UGA Y, SUGIMOTO K, OGAWA S, et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions[J]. Nature Genetics, 2013, 45(9): 1097−1102 doi: 10.1038/ng.2725
[7]	FRANKS S J, SIM S, WEIS A E. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation[J]. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(4): 1278−1282 doi: 10.1073/pnas.0608379104
[8]	ZIA R, NAWAZ M S, SIDDIQUE M J, et al. Plant survival under drought stress: Implications, adaptive responses, and integrated rhizosphere management strategy for stress mitigation[J]. Microbiological Research, 2021, 242: 126626 doi: 10.1016/j.micres.2020.126626
[9]	YU J, LAI Y M, WU X, et al. Overexpression of OsEm1 encoding a group I LEA protein confers enhanced drought tolerance in rice[J]. Biochemical and Biophysical Research Communications, 2016, 478(2): 703−709 doi: 10.1016/j.bbrc.2016.08.010
[10]	TYAGI R, PRADHAN S, BHATTACHARJEE A, et al. Management of abiotic stresses by microbiome-based engineering of the rhizosphere[J]. Journal of Applied Microbiology, 2022, 133(2): 254−272 doi: 10.1111/jam.15552
[11]	RYAN P R, DESSAUX Y, THOMASHOW L S, et al. Rhizosphere engineering and management for sustainable agriculture[J]. Plant and Soil, 2009, 321(1): 363−383
[12]	PÉREZ-JARAMILLO J E, MENDES R, RAAIJMAKERS J M. Impact of plant domestication on rhizosphere microbiome assembly and functions[J]. Plant Molecular Biology, 2016, 90(6): 635−644 doi: 10.1007/s11103-015-0337-7
[13]	LIU H W, BRETTELL L E, QIU Z G, et al. Microbiome-mediated stress resistance in plants[J]. Trends in Plant Science, 2020, 25(8): 733−743 doi: 10.1016/j.tplants.2020.03.014
[14]	CHENG S S, GONG X, XUE W F, et al. Plant-microbiome interactions: An eco-evolutionary perspective[J]. Biotechnology Bulletin, 2020, 36(9): 3−13
[15]	JALEEL C A, MANIVANNAN P, WAHID A, et al. Drought stress in plants: a review on morphological characteristics and pigments composition[J]. International Journal of Agriculture and Biology, 2009, 11(1): 100−105
[16]	WANG J F, WANG Y H, SONG X S, et al. Elevated atmospheric CO₂ and drought affect soil microbial community and functional diversity associated with Glycine max[J]. Revista Brasileira De Ciência Do Solo, 2017, 41: e0160460
[17]	SCHIMEL J P. Life in dry soils: effects of drought on soil microbial communities and processes[J]. Annual Review of Ecology, Evolution, and Systematics, 2018, 49: 409−432 doi: 10.1146/annurev-ecolsys-110617-062614
[18]	MANSOOR S, KHAN T, FAROOQ I, et al. Drought and global hunger: biotechnological interventions in sustainability and management[J]. Planta, 2022, 256(5): 97 doi: 10.1007/s00425-022-04006-x
[19]	AZARBAD H, CONSTANT P, GIARD-LALIBERTÉ C, et al. Water stress history and wheat genotype modulate rhizosphere microbial response to drought[J]. Soil Biology and Biochemistry, 2018, 126: 228−236 doi: 10.1016/j.soilbio.2018.08.017
[20]	FUCHSLUEGER L, BAHN M, FRITZ K, et al. Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow[J]. New Phytologist, 2014, 201(3): 916−927 doi: 10.1111/nph.12569
[21]	BREITKREUZ C, HERZIG L, BUSCOT F, et al. Interactions between soil properties, agricultural management and cultivar type drive structural and functional adaptations of the wheat rhizosphere microbiome to drought[J]. Environmental Microbiology, 2021, 23(10): 5866−5882 doi: 10.1111/1462-2920.15607
[22]	NOCKER A, FERNÁNDEZ P S, MONTIJN R, et al. Effect of air drying on bacterial viability: A multiparameter viability assessment[J]. Journal of Microbiological Methods, 2012, 90(2): 86−95 doi: 10.1016/j.mimet.2012.04.015
[23]	NAYLOR D, DEGRAAF S, PURDOM E, et al. Drought and host selection influence bacterial community dynamics in the grass root microbiome[J]. The ISME Journal, 2017, 11(12): 2691−270 doi: 10.1038/ismej.2017.118
[24]	WIPF M L, BÙI T N, COLEMAN-DERR D. Distinguishing between the impacts of heat and drought stress on the root microbiome of Sorghum bicolor[J]. Phytobiomes Journal, 2021, 5: 166−176 doi: 10.1094/PBIOMES-07-20-0052-R
[25]	XU L, DONG Z B, CHINIQUY D, et al. Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics[J]. Nature Communications, 2021, 12(1): 1−17 doi: 10.1038/s41467-020-20314-w
[26]	SANTOS-MEDELLÍN C, EDWARDS J, LIECHTY Z, et al. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes[J]. mBio, 2017, 8(4): e00764−e00717
[27]	MICKAN B S, ABBOTT L K, SOLAIMAN Z M, et al. Soil disturbance and water stress interact to influence arbuscular mycorrhizal fungi, rhizosphere bacteria and potential for N and C cycling in an agricultural soil[J]. Biology and Fertility of Soils, 2019, 55(1): 53−66 doi: 10.1007/s00374-018-1328-z
[28]	BESKROVNAYA P, SEXTON D L, GOLMOHAMMADZADEH M, et al. Structural, metabolic and evolutionary comparison of bacterial endospore and exospore formation[J]. Frontiers in Microbiology, 2021, 12: 630573 doi: 10.3389/fmicb.2021.630573
[29]	KEIBLINGER K M, HALL E K, WANEK W, et al. The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency[J]. FEMS Microbiology Ecology, 2010, 73(3): 430−440
[30]	WARD N L, CHALLACOMBE J F, JANSSEN P H, et al. Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils[J]. Applied and Environmental Microbiology, 2009, 75(7): 2046−2056 doi: 10.1128/AEM.02294-08
[31]	DE VRIES F T, GRIFFITHS R I, BAILEY M, et al. Soil bacterial networks are less stable under drought than fungal networks[J]. Nature Communications, 2018, 9(1): 1−12 doi: 10.1038/s41467-017-02088-w
[32]	HOPKINS A J M, RUTHROF K X, FONTAINE J B, et al. Forest die-off following global-change-type drought alters rhizosphere fungal communities[J]. Environmental Research Letters, 2018, 13(9): 095006 doi: 10.1088/1748-9326/aadc19
[33]	GAO C, MONTOYA L, XU L, et al. Fungal community assembly in drought-stressed sorghum shows stochasticity, selection, and universal ecological dynamics[J]. Nature Communications, 2020, 11(1): 1−14 doi: 10.1038/s41467-019-13993-7
[34]	CARBONE M J, ALANIZ S, MONDINO P, et al. Drought influences fungal community dynamics in the grapevine rhizosphere and root microbiome[J]. Journal of Fungi (Basel, Switzerland), 2021, 7(9): 686
[35]	CHIALVA M, GHIGNONE S, COZZI P, et al. Water management and phenology influence the root-associated rice field microbiota[J]. FEMS Microbiology Ecology, 2020, 96(9): fiaa146 doi: 10.1093/femsec/fiaa146
[36]	RUIZ-LOZANO J, PORCEL R, BÁRZANA G, et al. Contribution of arbuscular mycorrhizal symbiosis to plant drought tolerance: state of the art[M]//SANDERS G L, ARNDT S K. Plant Responses to Drought Stress. Berlin, Heidelberg: Springer, 2012: 335-362
[37]	MAITRA P, ZHENG Y, CHEN L, et al. Effect of drought and season on arbuscular mycorrhizal fungi in a subtropical secondary forest[J]. Fungal Ecology, 2019, 41: 107−115 doi: 10.1016/j.funeco.2019.04.005
[38]	TRESEDER K K, BERLEMONT R, ALLISON S D, et al. Drought increases the frequencies of fungal functional genes related to carbon and nitrogen acquisition[J]. PLoS One, 2018, 13(11): e0206441 doi: 10.1371/journal.pone.0206441
[39]	TRESEDER K K, LENNON J T. Fungal traits that drive ecosystem dynamics on land[J]. Microbiology and Molecular Biology Reviews:MMBR, 2015, 79(2): 243−262 doi: 10.1128/MMBR.00001-15
[40]	BAPIRI A, BÅÅTH E, ROUSK J. Drying-rewetting cycles affect fungal and bacterial growth differently in an arable soil[J]. Microbial Ecology, 2010, 60(2): 419−428 doi: 10.1007/s00248-010-9723-5
[41]	KUSVURAN S. Microalgae (Chlorella vulgaris Beijerinck) alleviates drought stress of broccoli plants by improving nutrient uptake, secondary metabolites, and antioxidative defense system[J]. Horticultural Plant Journal, 2021, 7(3): 221−231 doi: 10.1016/j.hpj.2021.03.007
[42]	KAHA M, IWAMOTO K, YAHYA N A, et al. Enhancement of astaxanthin accumulation using black light in Coelastrum and Monoraphidium isolated from Malaysia[J]. Scientific Reports, 2021, 11(1): 1−9 doi: 10.1038/s41598-020-79139-8
[43]	STEVNBAK K, SCHERBER C, GLADBACH D J, et al. Interactions between above- and below-ground organisms modified in climate change experiments[J]. Nature Climate Change, 2012, 2(11): 805−808 doi: 10.1038/nclimate1544
[44]	HRYNKIEWICZ K, BAUM C. The potential of rhizosphere microorganisms to promote the plant growth in disturbed soils[M]//MALK A, GROHMANN E. Environmental Protection Strategies for Sustainable Development. Dordrecht: Springer, 2012: 35–64
[45]	BANERJEE S, DUTTA S. Plant growth promoting activites of a fungal strain Penicillium commune MCC 1720 and it’s effect on growth of black gram[J]. The Pharma Innovation Journal, 2019, 8: 121−127
[46]	BATOOL T, ALI S, SELEIMAN M F, et al. Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities[J]. Scientific Reports, 2020, 10(1): 16975 doi: 10.1038/s41598-020-73489-z
[47]	ARZANESH M H, ALIKHANI H A, KHAVAZI K, et al. Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress[J]. World Journal of Microbiology and Biotechnology, 2011, 27(2): 197−205 doi: 10.1007/s11274-010-0444-1
[48]	MOLINA-FAVERO C, CREUS C M, SIMONTACCHI M, et al. Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato[J]. Molecular Plant-Microbe Interactions:MPMI, 2008, 21(7): 1001−1009 doi: 10.1094/MPMI-21-7-1001
[49]	ARMADA E, ROLDÁN A, AZCON R. Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plants species under drought conditions in natural arid soil[J]. Microbial Ecology, 2014, 67(2): 410−420 doi: 10.1007/s00248-013-0326-9
[50]	BARNAWAL D, BHARTI N, PANDEY S S, et al. Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression[J]. Physiologia Plantarum, 2017, 161(4): 502−514 doi: 10.1111/ppl.12614
[51]	LIM J H, KIM S D. Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper[J]. The Plant Pathology Journal, 2013, 29(2): 201−208 doi: 10.5423/PPJ.SI.02.2013.0021
[52]	UZMA M, IQBAL A, HASNAIN S. Drought tolerance induction and growth promotion by indole acetic acid producing Pseudomonas aeruginosa in Vigna radiata[J]. PLoS One, 2022, 17(2): e0262932 doi: 10.1371/journal.pone.0262932
[53]	LIU F C, XING S J, MA H L, et al. Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings[J]. Applied Microbiology and Biotechnology, 2013, 97(20): 9155−9164 doi: 10.1007/s00253-013-5193-2
[54]	ANSARY M H, RAHMANI H A, ARDAKAI M R, et al. Effect of Pseudomonas floresensent on proline and phytohormonal status of maize (Zea mays L.) under water deficit stress[J]. Annals of Biological Research, 2012, 3(2): 1054−1062
[55]	GLICK B R, CHENG Z Y, CZARNY J, et al. Promotion of plant growth by ACC deaminase-producing soil bacteria[J]. European Journal of Plant Pathology, 2007, 119(3): 329−339 doi: 10.1007/s10658-007-9162-4
[56]	AHMAD SHAKIR M, BANO A, ARSHAD A M. Short communication: Rhizosphere bacteria containing ACC-deaminase conferred drought tolerance in wheat grown under semi-arid climate[J]. Soil & Environment, 2012, 31(1): 108−112
[57]	ZAHIR Z A, MUNIR A, ASGHAR H N, et al. Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions[J]. Journal of Microbiology and Biotechnology, 2008, 18(5): 958−963
[58]	SALEEM A R, BRUNETTI C, KHALID A, et al. Drought response of Mucuna pruriens (L.) DC. inoculated with ACC deaminase and IAA producing rhizobacteria[J]. PLoS One, 2018, 13(2): e0191218 doi: 10.1371/journal.pone.0191218
[59]	ARSHAD M, SHAHAROONA B, MAHMOOD T. Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.)[J]. Pedosphere, 2008, 18(5): 611−620 doi: 10.1016/S1002-0160(08)60055-7
[60]	KHAN A, SINGH A V. Multifarious effect of ACC deaminase and EPS producing Pseudomonas sp. and Serratia marcescens to augment drought stress tolerance and nutrient status of wheat[J]. World Journal of Microbiology and Biotechnology, 2021, 37(12): 198 doi: 10.1007/s11274-021-03166-4
[61]	GILL S S, TUTEJA N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants[J]. Plant Physiology and Biochemistry, 2010, 48(12): 909−930 doi: 10.1016/j.plaphy.2010.08.016
[62]	MA X, XU Z C, LANG D Y, et al. Comprehensive physiological, transcriptomic, and metabolomic analyses reveal the synergistic mechanism of Bacillus pumilus G5 combined with silicon alleviate oxidative stress in drought-stressed Glycyrrhiza uralensis Fisch[J]. Frontiers in Plant Science, 2022, 13: 1033915 doi: 10.3389/fpls.2022.1033915
[63]	CHANDRA D, SRIVASTAVA R, GLICK B R, et al. Rhizobacteria producing ACC deaminase mitigate water-stress response in finger millet (Eleusine coracana (L.) Gaertn.)[J]. 3 Biotech, 2020, 10(2): 65 doi: 10.1007/s13205-019-2046-4
[64]	NARAYANASAMY S, THANGAPPAN S, UTHANDI S. Plant growth-promoting Bacillus sp. cahoots moisture stress alleviation in rice genotypes by triggering antioxidant defense system[J]. Microbiological Research, 2020, 239: 126518 doi: 10.1016/j.micres.2020.126518
[65]	WANG F, WEI Y L, YAN T Z, et al. Sphingomonas sp. Hbc-6 alters physiological metabolism and recruits beneficial rhizosphere bacteria to improve plant growth and drought tolerance[J]. Frontiers in Plant Science, 2022, 13: 1002772 doi: 10.3389/fpls.2022.1002772
[66]	XUE Z F, ZHAO S T, BOLD N, et al. Screening and characterization of two extracellular polysaccharide-producing bacteria from the biocrust of the mu us desert[J]. Molecules (Basel, Switzerland), 2021, 26(18): 5521 doi: 10.3390/molecules26185521
[67]	FITRIANI WANGSA PUTRIE R, TRI WAHYUDI A, ASIH NAWANGSIH A, et al. Screening of rhizobacteria for plant growth promotion and their tolerance to drought stress[J]. Microbiology Indonesia, 2013, 7(3): 94−104 doi: 10.5454/mi.7.3.2
[68]	HUSSAIN M B, ZAHIR Z, ASGHAR H, et al. Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat?[J]. International Journal of Agriculture and Biology, 2014, 16(1): 3−13
[69]	SANDHYA V, ALI S Z, GROVER M, et al. Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45[J]. Biology and Fertility of Soils, 2009, 46(1): 17−26 doi: 10.1007/s00374-009-0401-z
[70]	VURUKONDA S S K P, VARDHARAJULA S, SHRIVASTAVA M, et al. Multifunctional Pseudomonas putida strain FBKV₂ from arid rhizosphere soil and its growth promotional effects on maize under drought stress[J]. Rhizosphere, 2016, 1: 4−13 doi: 10.1016/j.rhisph.2016.07.005
[71]	KHAN N, BANO A, ZANDI P M. Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance[J]. Journal of Plant Interactions, 2018, 13(1): 239−247 doi: 10.1080/17429145.2018.1471527
[72]	JAHAGIRDAR S, KAMBREKAR D, NAVI S, et al. Plant Growth-Promoting Fungi: Diversity and Classification[M]. Switzerland AG: Spring, 2019: 25–34
[73]	ANWAR T, EL-MARAGHY S, HUSSEIN K. Plant protection properties of the Plant Growth-Promoting Fungi (PGPF): mechanisms and potentiality[J]. Fungal Biology, 2021, 11(1): 391−415
[74]	GUSAIN D Y, SINGH U, SHARMA A. Enhance activity of stress related enzymes in rice (Oryza sativa L.) induced by plant growth promoting fungi under drought stress[J]. African Journal of Agricultural Research, 2014, 9(19): 1430−1434 doi: 10.5897/AJAR2014.8575
[75]	PANDYA N D, DESAI P V, JADHAV H P, et al. Plant growth promoting potential of Aspergillus sp. NPF7, isolated from wheat rhizosphere in South Gujarat, India[J]. Environmental Sustainability, 2018, 1(3): 245−252 doi: 10.1007/s42398-018-0025-z
[76]	ISLAM S, AKANDA A M, SULTANA F, et al. Chilli rhizosphere fungus Aspergillus spp. PPA1 promotes vegetative growth of cucumber (Cucumis sativus) plants upon root colonisation[J]. Archives of Phytopathology and Plant Protection, 2014, 47(10): 1231−1238 doi: 10.1080/03235408.2013.837633
[77]	PANG Z Q, ZHAO Y, XU P, et al. Microbial diversity of upland rice roots and their influence on rice growth and drought tolerance[J]. Microorganisms, 2020, 8(9): 1329 doi: 10.3390/microorganisms8091329
[78]	SAXENA A, RAGHUWANSHI R, SINGH H B. Trichoderma species mediated differential tolerance against biotic stress of phytopathogens in Cicer arietinum L.[J]. Journal of Basic Microbiology, 2015, 55(2): 195−206 doi: 10.1002/jobm.201400317
[79]	DIXIT P, MUKHERJEE P K, RAMACHANDRAN V, et al. Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum[J]. PLoS One, 2011, 6(1): e16360 doi: 10.1371/journal.pone.0016360
[80]	NAZNIN H A, KIMURA M, MIYAZAWA M, et al. Analysis of volatile organic compounds emitted by plant growth-promoting fungus Phoma sp. GS8-3 for growth promotion effects on tobacco[J]. Microbes and Environments, 2013, 28(1): 42−49 doi: 10.1264/jsme2.ME12085
[81]	MATHUR S, TOMAR R S, JAJOO A. Arbuscular mycorrhizal fungi (AMF) protects photosynthetic apparatus of wheat under drought stress[J]. Photosynthesis Research, 2019, 139(1): 227−238
[82]	FERNÁNDEZ-LIZARAZO J C, MORENO-FONSECA L P. Mechanisms for tolerance to water-deficit stress in plants inoculated with arbuscular mycorrhizal fungi. A review[J]. Agronomía Colombiana, 2016, 34(2): 179−189
[83]	MA S P, BI Y L, ZHANG Y X, et al. Thermal infrared imaging study of water status and growth of arbuscular mycorrhizal soybean (Glycine max) under drought stress[J]. South African Journal of Botany, 2022, 146: 58−65 doi: 10.1016/j.sajb.2021.09.037
[84]	JABBOROVA D, ANNAPURNA K, AL-SADI A M, et al. Biochar and Arbuscular mycorrhizal fungi mediated enhanced drought tolerance in okra (Abelmoschus esculentus) plant growth, root morphological traits and physiological properties[J]. Saudi Journal of Biological Sciences, 2021, 28(10): 5490−5499 doi: 10.1016/j.sjbs.2021.08.016
[85]	BEGUM N, AHANGER M A, SU Y Y, et al. Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications[J]. Plants (Basel, Switzerland), 2019, 8(12): 579
[86]	WU Q S, XIA R X, ZOU Y N. Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress[J]. European Journal of Soil Biology, 2008, 44(1): 122−128 doi: 10.1016/j.ejsobi.2007.10.001
[87]	GONG M G, TANG M, CHEN H, et al. Effects of two Glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress[J]. New Forests, 2013, 44(3): 399−408 doi: 10.1007/s11056-012-9349-1
[88]	XIONG W, SONG Y Q, YANG K M, et al. Rhizosphere protists are key determinants of plant health[J]. Microbiome, 2020, 8(1): 27 doi: 10.1186/s40168-020-00799-9
[89]	ABD EL-BAKY H H, EL-BAZ F K, EL BAROTY G S. Enhancing antioxidant availability in wheat grains from plants grown under seawater stress in response to microalgae extract treatments[J]. Journal of the Science of Food and Agriculture, 2010, 90(2): 299−303 doi: 10.1002/jsfa.3815
[90]	OANCEA F, VELEA S, FATU V, et al. Micro-algae based plant biostimulant and its effect on water stressed tomato plants[J]. Romanian Journal of Plant Protection, 2013, VI: 104−117
[91]	MERCHUK-OVNAT L, FAHIMA T, EPHRATH J E, et al. Ancestral QTL alleles from wild emmer wheat enhance root development under drought in modern wheat[J]. Frontier in Plant Science, 2017, 8: 703 doi: 10.3389/fpls.2017.00703
[92]	HETRICK B A D, WILSON G W T, COX T S. Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors[J]. Canadian Journal of Botany, 2011, 70: 2032−2040
[93]	MARTÍN-ROBLES N, LEHMANN A, SECO E, et al. Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species[J]. New Phytologist, 2018, 218(1): 322−334 doi: 10.1111/nph.14962
[94]	CHANG J J, SUN Y, TIAN L, et al. The structure of rhizosphere fungal communities of wild and domesticated rice: changes in diversity and Co-occurrence patterns[J]. Frontiers in Microbiology, 2021, 12: 610823 doi: 10.3389/fmicb.2021.610823
[95]	LIU J G, YU X C, QIN Q L, et al. The impacts of domestication and breeding on nitrogen fixation symbiosis in legumes[J]. Frontiers in Genetics, 2020, 11: 00973 doi: 10.3389/fgene.2020.00973
[96]	KIERS E T, HUTTON M G, DENISON R F. Human selection and the relaxation of legume defences against ineffective rhizobia[J]. Proceedings of the Royal Society B:Biological Sciences, 2007, 274(1629): 3119−3126 doi: 10.1098/rspb.2007.1187
[97]	HAN Q, MA Q, CHEN Y, et al. Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean[J]. The ISME Journal, 2020, 14(8): 1915−1928 doi: 10.1038/s41396-020-0648-9
[98]	KIM D H, KAASHYAP M, RATHORE A, et al. Phylogenetic diversity of Mesorhizobium in chickpea[J]. Journal of Biosciences, 2014, 39(3): 513−517 doi: 10.1007/s12038-014-9429-9