应用遗传学与组学分析研究根系差异响应益生菌和病原菌机制

植物通过其根系固着生活在土壤环境中，而土壤环境是地球上微生物丰度最高的生态位之一。因此根系持续与大量共生微生物和潜在病原微生物长期共存。维持根际生态系统的健康是实现“藏粮于地，藏粮于技”战略的迫切需求。然而过去几十年的植物免疫学研究主要聚焦在叶片体系开展工作，人们对根系如何差异化识别和响应病原菌以及益生菌的分子特征和调控机制了解极少。解析根系与不同根际微生物的互作机制，有助于深入理解根系适应土壤微生物组的机制，为基于农业微生物组工程的可持续农业发展策略提供底层理论支持。

本研究旨在通过结合正向和反向遗传学方法，利用组学研究手段，解析根系与益生菌和病原菌差异化互作的分子特征和可能的调控因子。本研究首先构建了拟南芥根的单细胞转录图谱，揭示了根系细胞在面对模式益生菌假单胞菌WCS417和病原菌青枯菌GMI1000时的单细胞水平转录变化。通过单细胞RNA测序技术，我们在细胞亚型水平鉴定了根系对不同根系微生物的响应图谱，分别鉴定了1287个和2500个响应GMI1000和WCS417的基因。基因本体（GO）富集分析表明，这些差异表达基因主要参与了植物的免疫反应、低氧响应和硫代葡萄糖苷代谢等生物学过程。进一步地，我们利用加权共表达网络分析（WGCNA）技术，从单细胞数据中识别出16个细胞类型特异的基因模块，发现其中一些模块在不同处理下存在不同的响应强度。同时，我们预测到转录因子MYB59可能通过调控硫代葡萄糖苷代谢参与根系微生物响应，这些发现为理解植物-微生物互作提供了新的方向。此外，为了研究根系植保素相关代谢产物的调控机制，我们基于正向遗传学筛选，发现根系免疫突变体hsm4（hormone-mediated suppression of MAMP-triggered immunity 4）表现出增强的根系免疫表型，包括对病原菌青枯菌抗性和MAMP诱导的根系基础免疫响应的增强。转录组分析进一步揭示了hsm4突变体增强免疫的分子基础，包括免疫及毒素代谢相关基因的上调。最后通过微生物组测序分析发现HSM4能参与调控根系微生物组，综上结果表明HSM4在协同调控植物根系免疫和微生物组结构中起着关键作用。

综上所述，本研究不仅丰富了我们对植物根系免疫响应机制的理解，也有助于比较剖析根系差异化响应敌友的分子机制。通过揭示植物根系与不同微生物互作的保守性和特异性，我们的研究为综合利用遗传工程和微生物组工程技术，维持根系生态系统健康和促进农业可持续发展提供了理论储备。

[1] WHEELER T, VON BRAUN J. Climate change impacts on global food security [J]. Science (New York, NY), 2013, 341(6145): 508-13.
[2] ZHANG J, LIU Y-X, ZHANG N, et al. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice [J]. Nature Biotechnology, 2019, 37(6): 676-84.
[3] YANG J, KLOEPPER J W, RYU C-M. Rhizosphere bacteria help plants tolerate abiotic stress [J]. Trends in Plant Science, 2009, 14(1): 1-4.
[4] KWAK M-J, KONG H G, CHOI K, et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato [J]. Nature Biotechnology, 2018, 36(11): 1100-9.
[5] SONG Y, WILSON A J, ZHANG X C, et al. FERONIA restricts pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species [J]. Nature Plants, 2021, 7(5): 644-54.
[6] YU P, HE X, BAER M, et al. Plant flavones enrich rhizosphere oxalobacteraceae to improve maize performance under nitrogen deprivation [J]. Nature Plants, 2021, 7(4): 481-99.
[7] HARBORT C J, HASHIMOTO M, INOUE H, et al. Root-secreted coumarins and the microbiota interact to improve iron nutrition in arabidopsis [J]. Cell Host & Microbe, 2020, 28(6): 825-37.e6.
[8] TEIXEIRA P J P, COLAIANNI N R, FITZPATRICK C R, et al. Beyond pathogens: Microbiota interactions with the plant immune system [J]. Current Opinion in Microbiology, 2019, 49: 7-17.
[9] XIN X F, KVITKO B, HE S Y. Pseudomonas syringae: What it takes to be a pathogen [J]. Nature Reviews Microbiology, 2018, 16(5): 316-28.
[10] JONES J D, DANGL J L. The plant immune system [J]. Nature, 2006, 444(7117): 323-9.
[11] WEI WANG D T. Synergistic cooperation between cell surface and intracellular immune receptors potentiates to activate robust plant defense [J]. Chinese Bulletin of Botany, 2021, 56(2): 142-6.
[12] TANG D, WANG G, ZHOU J M. Receptor kinases in plant-pathogen interactions: More than pattern recognition [J]. The Plant Cell, 2017, 29(4): 618-37.
[13] SUN Y, LI L, MACHO A P, et al. Structural basis for flg22-induced activation of the arabidopsis FLS2-BAK1 immune complex [J]. Science (New York, NY), 2013, 342(6158): 624-8.
[14] ZHOU J M, ZHANG Y. Plant immunity: Danger perception and signaling [J]. Cell, 2020, 181(5): 978-89.
[15] GRANT M, BROWN I, ADAMS S, et al. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death [J]. The Plant Journal : For Cell and Molecular Biology, 2000, 23(4): 441-50.
[16] TORRES M A, JONES J D, DANGL J L. Reactive oxygen species signaling in response to pathogens [J]. Plant Physiology, 2006, 141(2): 373-8.
[17] DUBIELLA U, SEYBOLD H, DURIAN G, et al. Calcium-dependent protein kinase/nadph oxidase activation circuit is required for rapid defense signal propagation [J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(21): 8744-9.
[18] LI L, LI M, YU L, et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity [J]. Cell Host & Microbe, 2014, 15(3): 329-38.
[19] LU D, WU S, GAO X, et al. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity [J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(1): 496-501.
[20] TIAN W, HOU C, REN Z, et al. A calmodulin-gated calcium channel links pathogen patterns to plant immunity [J]. Nature, 2019, 572(7767): 131-5.
[21] SUN T, NITTA Y, ZHANG Q, et al. Antagonistic interactions between two map kinase cascades in plant development and immune signaling [J]. EMBO Reports, 2018, 19(7): e45324.
[22] ZHANG M, ZHANG S. Mitogen-activated protein kinase cascades in plant signaling [J]. Journal of Integrative Plant Biology, 2022, 64(2): 301-41.
[23] WAITE C, SCHUMACHER J, JOVANOVIC M, et al. Negative autogenous control of the master type III secretion system regulator hrpl in pseudomonas syringae [J]. mBio, 2017, 8(1).
[24] QI P, HUANG M, HU X, et al. A ralstonia solanacearum effector targets tga transcription factors to subvert salicylic acid signaling [J]. The Plant Cell, 2022, 34(5): 1666-83.
[25] BENT A F, MACKEY D. Elicitors, effectors, and r genes: The new paradigm and a lifetime supply of questions [J]. Annual Review of Phytopathology, 2007, 45: 399-436.
[26] WILLIAMS S J, YIN L, FOLEY G, et al. Structure and function of the tir domain from the grape NLR protein RPV1 [J]. Frontiers in Plant Science, 2016, 7: 1850.
[27] SUN Y, ZHU Y X, BALINT-KURTI P J, et al. Fine-tuning immunity: Players and regulators for plant NLRs [J]. Trends in Plant Science, 2020, 25(7): 695-713.
[28] JACOB F, VERNALDI S, MAEKAWA T. Evolution and conservation of plant NLR functions [J]. Frontiers in Immunology, 2013, 4: 297.
[29] KRASILEVA K V, DAHLBECK D, STASKAWICZ B J. Activation of an arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector [J]. The Plant Cell, 2010, 22(7): 2444-58.
[30] MA S, LAPIN D, LIU L, et al. Direct pathogen-induced assembly of an nlr immune receptor complex to form a holoenzyme [J]. Science (New York, NY), 2020, 370(6521).
[31] DANGL J L, JONES J D. Plant pathogens and integrated defence responses to infection [J]. Nature, 2001, 411(6839): 826-33.
[32] WU Y, GAO Y, ZHAN Y, et al. Loss of the common immune coreceptor BAK1 leads to NLR-dependent cell death [J]. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(43): 27044-53.
[33] NGOU B P M, AHN H-K, DING P, et al. Mutual potentiation of plant immunity by cell-surface and intracellular receptors [J]. Nature, 2021, 592(7852): 110-5.
[34] PRUITT R N, LOCCI F, WANKE F, et al. The EDS1–PAD4–ADR1 node mediates arabidopsis pattern-triggered immunity [J]. Nature, 2021, 598(7881): 495-9.
[35] TIAN H, WU Z, CHEN S, et al. Activation of tir signalling boosts pattern-triggered immunity [J]. Nature, 2021, 598(7881): 500-3.
[36] YUAN M, JIANG Z, BI G, et al. Pattern-recognition receptors are required for NLR-mediated plant immunity [J]. Nature, 2021, 592(7852): 105-9.
[37] STRINGLIS I A, PROIETTI S, HICKMAN R, et al. Root transcriptional dynamics induced by beneficial rhizobacteria and microbial immune elicitors reveal signatures of adaptation to mutualists [J]. The Plant Journal, 2018, 93(1): 166-80.
[38] TZIPILEVICH E, RUSS D, DANGL J L, et al. Plant immune system activation is necessary for efficient root colonization by auxin-secreting beneficial bacteria [J]. Cell Host & Microbe, 2021, 29(10): 1507-20.e4.
[39] COLAIANNI N R, PARYS K, LEE H S, et al. A complex immune response to flagellin epitope variation in commensal communities [J]. Cell Host & Microbe, 2021, 29(4): 635-49.e9.
[40] YU K, LIU Y, TICHELAAR R, et al. Rhizosphere-associated pseudomonas suppress local root immune responses by gluconic acid-mediated lowering of environmental pH [J]. Current Biology, 2019, 29(22): 3913-20.e4.
[41] FIORIN G L, SANCHéZ-VALLET A, DE TOLEDO THOMAZELLA D P, et al. Suppression of plant immunity by fungal chitinase-like effectors [J]. Current Biology, 2018, 28(18): 3023-30. e5.
[42] SáNCHEZ-VALLET A, MESTERS J R, THOMMA B P. The battle for chitin recognition in plant-microbe interactions [J]. FEMS Microbiology Reviews, 2015, 39(2): 171-83.
[43] STRINGLIS I A, ZAMIOUDIS C, BERENDSEN R L, et al. Type III secretion system of beneficial rhizobacteria pseudomonas simiae WCS417 and pseudomonas defensor WCS374 [J]. Frontiers in Microbiology, 2019, 10: 1631.
[44] MAVRODI D V, JOE A, MAVRODI O V, et al. Structural and functional analysis of the type III secretion system from pseudomonas fluorescens Q8r1-96 [J]. Journal of Bacteriology, 2011, 193(1): 177-89.
[45] REZZONICO F, BINDER C, DéFAGO G, et al. The type III secretion system of biocontrol pseudomonas fluorescens KD targets the phytopathogenic chromista pythium ultimum and promotes cucumber protection [J]. Molecular Plant-Microbe Interactions : MPMI, 2005, 18(9): 991-1001.
[46] YANG S, TANG F, GAO M, et al. R gene-controlled host specificity in the legume-rhizobia symbiosis [J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(43): 18735-40.
[47] ZHANG L, CHEN X-J, LU H-B, et al. Functional analysis of the type 3 effector nodulation outer protein l (nopl) from rhizobium sp. NGR234: Symbiotic effects, phosphorylation, and interference with mitogen-activated protein kinase signaling [J]. Journal of Biological Chemistry, 2011, 286(37): 32178-87.
[48] OKAZAKI S, KANEKO T, SATO S, et al. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system [J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(42): 17131-6.
[49] MA K W, NIU Y, JIA Y, et al. Coordination of microbe-host homeostasis by crosstalk with plant innate immunity [J]. Nature Plants, 2021, 7(6): 814-25.
[50] TEIXEIRA P, COLAIANNI N R, LAW T F, et al. Specific modulation of the root immune system by a community of commensal bacteria [J]. Proceedings of the National Academy of Sciences of the United States of America, 2021, 118(16).
[51] NGOU B P M, DING P, JONES J D G. Thirty years of resistance: Zig-zag through the plant immune system [J]. The Plant Cell, 2022, 34(5): 1447-78.
[52] WANG N R, HANEY C H. Harnessing the genetic potential of the plant microbiome [J]. The Biochemist, 2020, 42(4): 20-5.
[53] EMONET A, ZHOU F, VACHERON J, et al. Spatially restricted immune responses are required for maintaining root meristematic activity upon detection of bacteria [J]. Current Biology, 2021, 31(5): 1012-28.e7.
[54] ZHOU F, EMONET A, DéNERVAUD TENDON V, et al. Co-incidence of damage and microbial patterns controls localized immune responses in roots [J]. Cell, 2020, 180(3): 440-53.e18.
[55] MILLET Y A, DANNA C H, CLAY N K, et al. Innate immune responses activated in arabidopsis roots by microbe-associated molecular patterns [J]. The Plant Cell, 2010, 22(3): 973-90.
[56] ZHENG X Y, SPIVEY N W, ZENG W, et al. Coronatine promotes pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation [J]. Cell Host & Microbe, 2012, 11(6): 587-96.
[57] DE SMET S, CUYPERS A, VANGRONSVELD J, et al. Gene networks involved in hormonal control of root development in arabidopsis thaliana: A framework for studying its disturbance by metal stress [J]. International Journal of Molecular Sciences, 2015, 16(8): 19195-224.
[58] VERBON E H, LIBERMAN L M, ZHOU J, et al. Cell-type-specific transcriptomics reveals that root hairs and endodermal barriers play important roles in beneficial plant-rhizobacterium interactions [J]. Molecular Plant, 2023, 16(7): 1160-77.
[59] BECK M, WYRSCH I, STRUTT J, et al. Expression patterns of FLAGELLIN SENSING 2 map to bacterial entry sites in plant shoots and roots [J]. Journal of Experimental Botany, 2014, 65(22): 6487-98.
[60] RICH-GRIFFIN C, EICHMANN R, REITZ M U, et al. Regulation of cell type-specific immunity networks in arabidopsis roots [J]. The Plant Cell, 2020, 32(9): 2742-62.
[61] 朱忠旭, 陈新. 单细胞测序技术及应用进展 [J]. 基因组学与应用生物学, 2015, 34(05): 902-8.
[62] TANG F, BARBACIORU C, WANG Y, et al. mRna-seq whole-transcriptome analysis of a single cell [J]. Nature Methods, 2009, 6(5): 377-82.
[63] MACOSKO E Z, BASU A, SATIJA R, et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets [J]. Cell, 2015, 161(5): 1202-14.
[64] DENYER T, MA X, KLESEN S, et al. Spatiotemporal developmental trajectories in the arabidopsis root revealed using high-throughput single-cell rna sequencing [J]. Developmental Cell, 2019, 48(6): 840-52.e5.
[65] JEAN-BAPTISTE K, MCFALINE-FIGUEROA J L, ALEXANDRE C M, et al. Dynamics of gene expression in single root cells of arabidopsis thaliana [J]. The Plant Cell, 2019, 31(5): 993-1011.
[66] RYU K H, HUANG L, KANG H M, et al. Single-cell rna sequencing resolves molecular relationships among individual plant cells [J]. Plant Physiology, 2019, 179(4): 1444-56.
[67] SHAHAN R, HSU C-W, NOLAN T M, et al. A single-cell arabidopsis root atlas reveals developmental trajectories in wild-type and cell identity mutants [J]. Developmental Cell, 2022, 57(4): 543-60. e9.
[68] ZHANG B, GAO Y, ZHANG L, et al. The plant cell wall: Biosynthesis, construction, and functions [J]. Journal of Integrative Plant Biology, 2021, 63(1): 251-72.
[69] BIRNBAUM K, SHASHA D E, WANG J Y, et al. A gene expression map of the arabidopsis root [J]. Science (New York, NY), 2003, 302(5652): 1956-60.
[70] SHULSE C N, COLE B J, CIOBANU D, et al. High-throughput single-cell transcriptome profiling of plant cell types [J]. Cell Reports, 2019, 27(7): 2241-7. e4.
[71] LIANG Q, DHARMAT R, OWEN L, et al. Single-nuclei rna-seq on human retinal tissue provides improved transcriptome profiling [J]. Nature Communications, 2019, 10(1): 5743.
[72] KALISH B T, BARKAT T R, DIEL E E, et al. Single-nucleus rna sequencing of mouse auditory cortex reveals critical period triggers and brakes [J]. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(21): 11744-52.
[73] FARMER A, THIBIVILLIERS S, RYU K H, et al. The impact of chromatin remodeling on gene expression at the single cell level in arabidopsis thaliana [J]. bioRxiv, 2020: 2020.07. 27.223156.
[74] ZHANG T Q, XU Z G, SHANG G D, et al. A single-cell rna sequencing profiles the developmental landscape of arabidopsis root [J]. Molecular Plant, 2019, 12(5): 648-60.
[75] WENDRICH J R, YANG B, VANDAMME N, et al. Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions [J]. Science, 2020, 370(6518): eaay4970.
[76] LIU Z, KONG X, LONG Y, et al. Integrated single-nucleus and spatial transcriptomics captures transitional states in soybean nodule maturation [J]. Nature Plants, 2023, 9(4): 515-24.
[77] ZHU J, LOLLE S, TANG A, et al. Single-cell profiling of arabidopsis leaves to pseudomonas syringae infection [J]. Cell Reports, 2023, 42(7): 112676.
[78] TANG B, FENG L, HULIN M T, et al. Cell-type-specific responses to fungal infection in plants revealed by single-cell transcriptomics [J]. Cell Host & Microbe, 2023, 31(10): 1732-47.e5.
[79] STRINGLIS I A, YU K, FEUSSNER K, et al. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health [J]. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(22): E5213-e22.
[80] HUANG A C, JIANG T, LIU Y X, et al. A specialized metabolic network selectively modulates arabidopsis root microbiota [J]. Science (New York, NY), 2019, 364(6440).
[81] HIRUMA K, GERLACH N, SACRISTáN S, et al. Root endophyte colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent [J]. Cell, 2016, 165(2): 464-74.
[82] CASTRILLO G, TEIXEIRA P J, PAREDES S H, et al. Root microbiota drive direct integration of phosphate stress and immunity [J]. Nature, 2017, 543(7646): 513-8.
[83] CHIAPPERO J, DEL ROSARIO CAPPELLARI L, ALDERETE L G S, et al. Plant growth promoting rhizobacteria improve the antioxidant status in mentha piperita grown under drought stress leading to an enhancement of plant growth and total phenolic content [J]. Industrial Crops Products, 2019, 139: 111553.
[84] PIETERSE C M, BERENDSEN R L, DE JONGE R, et al. Pseudomonas simiae WCS417: Star track of a model beneficial rhizobacterium [J]. Plant Soil, 2021, 461: 245-63.
[85] LI C-H, WANG K-C, HONG Y-H, et al. Roles of different forms of lipopolysaccharides in ralstonia solanacearum pathogenesis [J]. Molecular Plant-Microbe Interactions, 2014, 27(5): 471-8.
[86] JIANG G, WEI Z, XU J, et al. Bacterial wilt in china: History, current status, and future perspectives [J]. Frontiers in Plant Science, 2017, 8: 1549.
[87] WOLF F A, ANGERER P, THEIS F J. Scanpy: Large-scale single-cell gene expression data analysis [J]. Genome Biology, 2018, 19(1): 15.
[88] GERMAIN P L, LUN A, GARCIA MEIXIDE C, et al. Doublet identification in single-cell sequencing data using scdblfinder [J]. F1000Research, 2021, 10: 979.
[89] HAO Y, HAO S, ANDERSEN-NISSEN E, et al. Integrated analysis of multimodal single-cell data [J]. Cell, 2021, 184(13): 3573-87.e29.
[90] MCINNES L, HEALY J, MELVILLE J. UMAP: Uniform manifold approximation and projection for dimension reduction [J]. arXiv, 2018: arXiv:1802.03426.
[91] WU T, HU E, XU S, et al. ClusterProfiler 4.0: A universal enrichment tool for interpreting omics data [J]. Innovation (Cambridge (Mass)), 2021, 2(3): 100141.
[92] LANGFELDER P, HORVATH S. WGCNA: An R package for weighted correlation network analysis [J]. BMC Bioinformatics, 2008, 9: 559.
[93] AMRINE K C, BLANCO-ULATE B, CANTU D. Discovery of core biotic stress responsive genes in arabidopsis by weighted gene co-expression network analysis [J]. PloS One, 2015, 10(3): e0118731.
[94] ZHU M, XIE H, WEI X, et al. WGCNA analysis of salt-responsive core transcriptome identifies novel hub genes in rice [J]. Genes, 2019, 10(9): 719.
[95] HE Y, WANG Z, GE H, et al. Weighted gene co-expression network analysis identifies genes related to anthocyanin biosynthesis and functional verification of hub gene SmWRKY44 [J]. Plant Science, 2021, 309: 110935.
[96] LIU Z, YANG J, LONG Y, et al. Single-nucleus transcriptomes reveal spatiotemporal symbiotic perception and early response in medicago [J]. Nature Plants, 2023, 9(10): 1734-48.
[97] MORABITO S, REESE F, RAHIMZADEH N, et al. HdWGCNA identifies co-expression networks in high-dimensional transcriptomics data [J]. Cell Reports Methods, 2023, 3(6): 100498.
[98] ZHAO C, WANG H, LU Y, et al. Deep sequencing reveals early reprogramming of arabidopsis root transcriptomes upon ralstonia solanacearum infection [J]. Molecular Plant-Microbe Interactions, 2019, 32(7): 813-27.
[99] MARRS K A. The functions and regulation of glutathione s-transferases in plants [J]. Annual Review of Plant Physiology and Plant Molecular Biology, 1996, 47: 127-58.
[100] SALAS-GONZáLEZ I, REYT G, FLIS P, et al. Coordination between microbiota and root endodermis supports plant mineral nutrient homeostasis [J]. Science (New York, NY), 2021, 371(6525): eabd0695.
[101] SHUKLA V, BARBERON M. Building and breaking of a barrier: Suberin plasticity and function in the endodermis [J]. Current Opinion in Plant Biology, 2021, 64: 102153.
[102] DEL CARMEN MARTíNEZ-BALLESTA M, MORENO D A, CARVAJAL M. The physiological importance of glucosinolates on plant response to abiotic stress in brassica [J]. International Journal of Molecular Sciences, 2013, 14(6): 11607-25.
[103] THOMMA B P, NELISSEN I, EGGERMONT K, et al. Deficiency in phytoalexin production causes enhanced susceptibility of arabidopsis thaliana to the fungus alternaria brassicicola [J]. The Plant Journal, 1999, 19(2): 163-71.
[104] ORTIZ A, SANSINENEA E. Phenylpropanoid derivatives and their role in plants' health and as antimicrobials [J]. Current Microbiology, 2023, 80(12): 380.
[105] MIEDES E, VANHOLME R, BOERJAN W, et al. The role of the secondary cell wall in plant resistance to pathogens [J]. Frontiers in Plant Science, 2014, 5: 358.
[106] LORETI E, PERATA P. The many facets of hypoxia in plants [J]. Plants (Basel, Switzerland), 2020, 9(6).
[107] VALERI M C, NOVI G, WEITS D A, et al. Botrytis cinerea induces local hypoxia in arabidopsis leaves [J]. The New Phytologist, 2021, 229(1): 173-85.
[108] KOPRIVOVA A, SCHUCK S, JACOBY R P, et al. Root-specific camalexin biosynthesis controls the plant growth-promoting effects of multiple bacterial strains [J]. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(31): 15735-44.
[109] YANG L, ZHANG Y, GUAN R, et al. Co-regulation of indole glucosinolates and camalexin biosynthesis by CPK5/CPK6 and MPK3/MPK6 signaling pathways [J]. Journal of Integrative Plant Biology, 2020, 62(11): 1780-96.
[110] LIU Y, WILSON A J, HAN J, et al. Amino acid availability determines plant immune homeostasis in the rhizosphere microbiome [J]. mBio, 2023, 14(2): e03424-22.
[111] PAASCH B C, SOHRABI R, KREMER J M, et al. A critical role of a eubiotic microbiota in gating proper immunocompetence in arabidopsis [J]. Nature Plants, 2023, 9(9): 1468-80.
[112] ZHANG X C, MILLET Y A, CHENG Z, et al. Jasmonate signalling in arabidopsis involves SGT1B-HSP70-HSP90 chaperone complexes [J]. Nature Plants, 2015, 1.
[113] SONG Y, ZHANG X-C, QIU Y, et al. A screen for mutants deficient in coronatine-mediated suppression of root immunity identifies arabidopsis SDA1 as a novel integrator of immunity and phytohormone signaling [J]. bioRxiv, 2021: 2021.09.12.459990.
[114] SCHWESSINGER B, ROUX M, KADOTA Y, et al. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1 [J]. PLoS Genetics, 2011, 7(4): e1002046.
[115] PATRO R, DUGGAL G, LOVE M I, et al. Salmon provides fast and bias-aware quantification of transcript expression [J]. Nature Methods, 2017, 14(4): 417-9.
[116] CHEN S, ZHOU Y, CHEN Y, et al. Fastp: An ultra-fast all-in-one fastq preprocessor [J]. Bioinformatics, 2018, 34(17): i884-i90.
[117] KECHIN A, BOYARSKIKH U, KEL A, et al. Cutprimers: A new tool for accurate cutting of primers from reads of targeted next generation sequencing [J]. Journal of Computational Biology, 2017, 24(11): 1138-43.
[118] BOLYEN E, RIDEOUT J R, DILLON M R, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 [J]. Nature Biotechnol, 2019, 37(8): 852-7.
[119] SONG S, MORALES MOREIRA Z, BRIGGS A L, et al. PSKR1 balances the plant growth–defence trade-off in the rhizosphere microbiome [J]. Nature Plants, 2023, 9(12): 2071-84.
[120] HARRIS J M, BALINT-KURTI P, BEDE J C, et al. What are the top 10 unanswered questions in molecular plant-microbe interactions? [J]. Molecular Plant-Microbe Interactions, 2020, 33(12): 1354-65.
[121] LEóN J, CASTILLO M C, GAYUBAS B. The hypoxia-reoxygenation stress in plants [J]. Journal of Experimental Botany, 2021, 72(16): 5841-56.
[122] KERPEN L, NICCOLINI L, LICAUSI F, et al. Hypoxic conditions in crown galls induce plant anaerobic responses that support tumor proliferation [J]. Frontiers in Plant Science, 2019, 10: 427736.
[123] MOONEY B C, DOORLY C M, MANTZ M, et al. Repression of pattern-triggered immune responses by hypoxia [J]. bioRxiv, 2023: 2023.11.07.565979.
[124] JELENSKA J, VAN HAL J A, GREENBERG J T. Pseudomonas syringae hijacks plant stress chaperone machinery for virulence [J]. Proceedings of the National Academy of Sciences, 2010, 107(29): 13177-82.
[125] MAIMBO M, OHNISHI K, HIKICHI Y, et al. Induction of a small heat shock protein and its functional roles in nicotiana plants in the defense response against ralstonia solanacearum [J]. Plant Physiology, 2007, 145(4): 1588-99.
[126] PANGESTI N, REICHELT M, VAN DE MORTEL J E, et al. Jasmonic acid and ethylene signaling pathways regulate glucosinolate levels in plants during rhizobacteria-induced systemic resistance against a leaf-chewing herbivore [J]. Journal of Chemical Ecology, 2016, 42(12): 1212-25.
[127] AUGUSTIN J M, KUZINA V, ANDERSEN S B, et al. Molecular activities, biosynthesis and evolution of triterpenoid saponins [J]. Phytochemistry, 2011, 72(6): 435-57.
[128] ZHONG Y, XUN W, WANG X, et al. Root-secreted bitter triterpene modulates the rhizosphere microbiota to improve plant fitness [J]. Nature Plants, 2022, 8(8): 887-96.
[129] MIAO H, CAI C, WEI J, et al. Glucose enhances indolic glucosinolate biosynthesis without reducing primary sulfur assimilation [J]. Scientific Reports, 2016, 6(1): 31854.
[130] DU X-Q, WANG F-L, LI H, et al. The transcription factor MYB59 regulates K+/NO3− translocation in the arabidopsis response to low K+ stress [J]. The Plant Cell, 2019, 31(3): 699-714.
[131] WIŚNIEWSKA A, WOJSZKO K, RóŻAŃSKA E, et al. Arabidopsis thaliana MYB59 gene is involved in the response to heterodera schachtii infestation, and its overexpression disturbs regular development of nematode-induced syncytia [J]. International Journal of Molecular Sciences, 2021, 22(12).