Multi-omics Approaches to Improve the Studies on the Mechanisms of Clubroot Resistance in Brassica Hosts

doi:10.16420/j.issn.0513-353x.2025-0153

Acta Horticulturae Sinica ›› 2025, Vol. 52 ›› Issue (5): 1213-1232.doi: 10.16420/j.issn.0513-353x.2025-0153

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Multi-omics Approaches to Improve the Studies on the Mechanisms of Clubroot Resistance in Brassica Hosts

ZHENG Jingyi, LI Xiaonan^*(), PIAO Zhongyun^*()

College of Horticulture，Shenyang Agricultural University，Shenyang 110866，China

Received:2025-04-23 Revised:2025-05-12 Online:2025-05-23 Published:2025-05-21
Contact: LI Xiaonan, PIAO Zhongyun

Abstract

Abstract:

Clubroot，caused by the obligate biotrophic protist Plasmodiophora brassicae Woronin，is a soil-borne pathogen that has emerged as one of the most devastating diseases in global Brassica crop production. Notably，the geographical distribution of infected areas has exhibited a significant expansion trend in recent years. Therefore，systematically elucidating the molecular pathogenesis of P. brassicae and the regulatory mechanisms of host immune response networks in Brassica species is critical for breeding resistant cultivars and establishing integrated disease management systems. Currently，leveraging breakthroughs in high-throughput sequencing technologies and the exponential growth of multi-omics data，researchers have unveiled the molecular atlas of the P. brassicae-Brassica host interaction interface from multidimensional perspectives. This review comprehensively synthesizes key advancements in the field，with a focus on the pivotal role of integrated multi-omics approaches in deciphering the pathogen’s biological characteristics，genetic mapping of resistance genes，and decoding host-pathogen interaction mechanisms. The findings aim to provide theoretical foundations and technical pathways for developing targeted molecular breeding strategies and innovative disease control strategies against clubroot.

Key words: Brassica, clubroot, Plasmodiophora brassicae, omics

ZHENG Jingyi, LI Xiaonan, PIAO Zhongyun. Multi-omics Approaches to Improve the Studies on the Mechanisms of Clubroot Resistance in Brassica Hosts[J]. Acta Horticulturae Sinica, 2025, 52(5): 1213-1232.

Figures/Tables 8

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寄主编号 Number	寄主来源 Host	二进制 Binary number series	十进制 Denary number series	寄主编号 Number	寄主来源 Host	二进制 Binary number series	十进制 Denary number series
	Brassica rapa L. Sensu lato，2n = 20				Brassica napus L.，2n = 38
ECD01	ssp. rapifera line aaBBCC	2⁰	1	ECD06	var. napus line Dc101	2⁰	1
ECD02	ssp. rapifera line AAbbCC	2¹	2	ECD07	var. napus line Dc119	2¹	2
ECD03	ssp. rapifera line AABBcc	2²	4	ECD08	var. napus line Dc128	2²	4
ECD04	ssp. rapifera line AABBCC	2³	8	ECD09	var. napus line Dc129	2³	8
ECD05	ssp. pekinensis‘Granaat’	2⁴	16	ECD10	var. napus line Dc130	2⁴	16
	Brassica oleracea L.，2n = 18
ECD11	var. capitata‘Badger Shipper’	2⁰	1
ECD12	var. capitata‘Bindsachsener’	2¹	2
ECD13	var. capitata‘Jersey Queen’	2²	4
ECD14	var. capitata‘Septa’	2³	8
ECD15	var. acephala subvar. laciniata‘Verheul’	2⁴	16

寄主编号 Number	寄主来源 Host	二进制 Binary number series	十进制 Denary number series	寄主编号 Number	寄主来源 Host	二进制 Binary number series	十进制 Denary number series
	Brassica rapa L. Sensu lato，2n = 20				Brassica napus L.，2n = 38
ECD01	ssp. rapifera line aaBBCC	2⁰	1	ECD06	var. napus line Dc101	2⁰	1
ECD02	ssp. rapifera line AAbbCC	2¹	2	ECD07	var. napus line Dc119	2¹	2
ECD03	ssp. rapifera line AABBcc	2²	4	ECD08	var. napus line Dc128	2²	4
ECD04	ssp. rapifera line AABBCC	2³	8	ECD09	var. napus line Dc129	2³	8
ECD05	ssp. pekinensis‘Granaat’	2⁴	16	ECD10	var. napus line Dc130	2⁴	16
	Brassica oleracea L.，2n = 18
ECD11	var. capitata‘Badger Shipper’	2⁰	1
ECD12	var. capitata‘Bindsachsener’	2¹	2
ECD13	var. capitata‘Jersey Queen’	2²	4
ECD14	var. capitata‘Septa’	2³	8
ECD15	var. acephala subvar. laciniata‘Verheul’	2⁴	16

鉴定系统 Classification system	生理小种 Pathotype designation
CCD	A	B	C	D	E	F	G	H	I	J	K	L	M	N	O	P	X
Williams	3	2	5	3	8	2	5	3	5	8	5	5	6	8	3	8	5
Somé	P₂	P₂	P₂	P₂	P₂	P₂	P₃	P₂	P₂	P₃	P₃	P₃	P₂	P₂	P₃	P₂	P₃
寄主Differential host	抗性反应Reaction
ECD 02	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
ECD 05	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+
ECD 06	+	+	+	+	+	+	-	+	+	-	-	-	+	+	-	+	-
ECD 08	+	+	+	+	+	+	+	+	+	+	-	+	+	+	+	+	+
ECD 09	+	+	+	+	+	+	-	+	+	-	-	-	+	+	+	+	-
ECD 10	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
ECD 11	-		-	-	-	+	-	-	-	-	-	-	-	-	-	-	-
ECD 13	+	+	-	+	-	+	-	+	-	-	-	-	+	-	-	-	-
Brutor	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+
Laurentian	+	+	-	+	+	+	-	+	-	+	-	-	-	+	+	+	-
Mendel	+	+	-	-	-	-	-	-	-	-	-	-	-	-	-	+	+
Westar	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+
45H29	+	+	+	+	+	-	+	-	-	+	+	-	-	-	+	+	+

鉴定系统 Classification system	生理小种 Pathotype designation
CCD	A	B	C	D	E	F	G	H	I	J	K	L	M	N	O	P	X
Williams	3	2	5	3	8	2	5	3	5	8	5	5	6	8	3	8	5
Somé	P₂	P₂	P₂	P₂	P₂	P₂	P₃	P₂	P₂	P₃	P₃	P₃	P₂	P₂	P₃	P₂	P₃
寄主Differential host	抗性反应Reaction
ECD 02	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
ECD 05	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+
ECD 06	+	+	+	+	+	+	-	+	+	-	-	-	+	+	-	+	-
ECD 08	+	+	+	+	+	+	+	+	+	+	-	+	+	+	+	+	+
ECD 09	+	+	+	+	+	+	-	+	+	-	-	-	+	+	+	+	-
ECD 10	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
ECD 11	-		-	-	-	+	-	-	-	-	-	-	-	-	-	-	-
ECD 13	+	+	-	+	-	+	-	+	-	-	-	-	+	-	-	-	-
Brutor	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+
Laurentian	+	+	-	+	+	+	-	+	-	+	-	-	-	+	+	+	-
Mendel	+	+	-	-	-	-	-	-	-	-	-	-	-	-	-	+	+
Westar	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+
45H29	+	+	+	+	+	-	+	-	-	+	+	-	-	-	+	+	+

寄主Host	Pb1	Pb2	Pb3	Pb4	Pb5	Pb6	Pb7	Pb8	Pb9	Pb10	Pb11	Pb12	Pb13	Pb14	Pb15	Pb16
H01	-	-	-	-	-	-	-	-	-	+	-	-	-	-	-	-
H02	-	-	-	-	-	-	-	-	+	+	+	-	-	+	+	+
H03	-	-	-	-	-	-	+	+	+	+	+	-	-	-	+	-
H04	-	-	-	-	-	+	-	+	+	+	+	-	+	-	+	+
H05	-	-	-	+	+	+	-	+	-	-	+	-	-	+	+	+
H06	-	-	-	+	-	-	-	-	-	-	+	+	-	+	-	+
H07	-	-	+	-	-	-	-	-	-	-	-	-	+	-	-	-
H08	-	+	-	-	-	-	-	-	-	-	-	-	-	-	-	-
H09	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+

Multi-omics Approaches to Improve the Studies on the Mechanisms of Clubroot Resistance in Brassica Hosts

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寄主 Host	生理小种 Pb. Race
寄主 Host	1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16
Jersey Queen	+	+	+	+	-	+	+	-	-	+	-	+	-	-	-	-
Badger Shipper	-	+	-	+	-	-	+	-	-	+	+	-	+	+	+	-
Laurentian	+	+	+	+	-	-	-	+	+	-	+	-	+	-	-	-
Wilhelmsburger	+	-	-	+	-	-	-	-	+	+	+	+	-	+	-	+

寄主Host	Pb1	Pb2	Pb3	Pb4	Pb5	Pb6	Pb7	Pb8	Pb9	Pb10	Pb11	Pb12	Pb13	Pb14	Pb15	Pb16
H01	-	-	-	-	-	-	-	-	-	+	-	-	-	-	-	-
H02	-	-	-	-	-	-	-	-	+	+	+	-	-	+	+	+
H03	-	-	-	-	-	-	+	+	+	+	+	-	-	-	+	-
H04	-	-	-	-	-	+	-	+	+	+	+	-	+	-	+	+
H05	-	-	-	+	+	+	-	+	-	-	+	-	-	+	+	+
H06	-	-	-	+	-	-	-	-	-	-	+	+	-	+	-	+
H07	-	-	+	-	-	-	-	-	-	-	-	-	+	-	-	-
H08	-	+	-	-	-	-	-	-	-	-	-	-	-	-	-	-
H09	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+

寄主Host	Pb1	Pb2	Pb3	Pb4	Pb5	Pb6	Pb7	Pb8	Pb9	Pb10	Pb11	Pb12	Pb13	Pb14	Pb15	Pb16
H01	-	-	-	-	-	-	-	-	-	+	-	-	-	-	-	-
H02	-	-	-	-	-	-	-	-	+	+	+	-	-	+	+	+
H03	-	-	-	-	-	-	+	+	+	+	+	-	-	-	+	-
H04	-	-	-	-	-	+	-	+	+	+	+	-	+	-	+	+
H05	-	-	-	+	+	+	-	+	-	-	+	-	-	+	+	+
H06	-	-	-	+	-	-	-	-	-	-	+	+	-	+	-	+
H07	-	-	+	-	-	-	-	-	-	-	-	-	+	-	-	-
H08	-	+	-	-	-	-	-	-	-	-	-	-	-	-	-	-
H09	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+

抗病位点Locus	染色体Chr.	侧翼标记Flanking marker	抗性来源Source	参考文献Reference
Crr1	A08	BRMS-088-SSR	Siloga	Suwabe et al.,2003
Crr1a	A08	BSA7，BRMS-088	Siloga	Suwabe et al.,2006； Hatakeyama et al.,2013
Crr1b	A08	BSA2，AT27	Siloga	Hatakeyama et al.,2013
Crr2	A01	BRMS-100-SSR，BRMS-096-SSR	Siloga	Suwabe et al.,2003
Crr3	A02	OPC11-1-1-STS，BrSTS-33	Milan white	Saito et al.,2006
Crr4	A06	BN288D-RFLP，WE24-1-RAPD	Siloga	Suwabe et al.,2006
Crr5	A08	Crr5-funK3	ECD01	Yang et al.,2025
CrrA5	A05	tau_cBrCR404	Inbreed line 20-2cc1	Nguyen et al.,2018
CR6a	A01		KU-101	Lee et al.,2002
CR6b	A03		KU-101	Lee et al.,2002
CRa	A03	HC352b-SCAR	DH line T136-8	Matsumoto et al.,1998；Ueno et al.,2012
CRb	A03	TCR09-SCAR，TCR79-TCR108	CR Shinki	Zhang et al.,2014
CRb^kato	A03	TCR02	CR Shinki	Kato et al.,2012,2013
CRc	A02	OPC11-1-STS，BrSTS-33	Debra	Sakamoto et al.,2008
CRd	A03	BRSTS61	Line 85-74	Pang et al.,2018
CRk	A03	HC688-RFLP，OPC11-2S-STS	Debra	Sakamoto et al.,2008
CRq	A03	BrQ-2-Indel	Chinese cabbage	Yuan & Wei,2015
CRs	A08	SNP-11505101	Akimeki	Laila et al.,2019
Rcr1	A03	SNP_A03-16	Flower Nabana	Yu et al.,2016
Rcr2	A03	SNP_A03-67	Jazz	Huang et al.,2017
Rcr3	A08	A90_A08_SNP_M12 and M16	Waaslander	Karim et al.,2020
Rcr4	A03	A03_22692045，A03_25649385	T19	Yu et al.,2017
Rcr5	A03	SNP_A03-83，SNP_A03_100	Purple Top White Globe	Huang et al.,2019
Rcr8	A02	A02_18503233，A02_22097179	T19	Yu et al.,2017
Rcr9	A08	A08_7105657，A08_13587639	T19	Yu et al.,2017
Rcr9^wa	A08	A90_A08_SNP_M28 and M79	Waaslander（derivation of ECD04）	Karim et al.,2020
PbBa3.1	A03	sau_um438a	ECD04	Chen et al.,2013
PbBa3.3	A03	sau_um398a	ECD04	Chen et al.,2013
PbBa8.1	A08	cnu_m490a	ECD04	Chen et al.,2013
BraPb8.3	A08	srt8-65，srt8-25	377	Kong et al.,2024
qBrCR38-1	A07	Br_K_07106，Br_K_07107	CR38	Zhu et al.,2019
qBrCR38-2	A08	Br_K_080103，Br_K_080107	CR38	Zhu et al.,2019
QS_B1.1	A01	BRMS287-aaf_SN3523a	Siloga	Pang et al.,2015
QS_B3.1	A03	sau_um028-At4g35530	Siloga	Pang et al.,2015
QS_B8.1	A08	BRPGM0920-BRPGM0173	Siloga	Pang et al.,2015
CRA8.1 CRA3.7	A08 A03	A08-4346，A08-4853 syau-InDel3024，syau-InDel3008	DW CR510（derivation of Siloga）	Wang et al.,2022a Pang et al.,2022

效应物 Effector	功能解析描述 Putative annotated function	参考文献 Reference
PbBSMT	SABATH型甲基转移酶，将水杨酸转化为水杨酸甲酯 SABATH group of methyltransferases，responsible for methylating endogenous salicylic acid (SA) in plants to form methyl salicylate (MeSA)	Ludwig-Müller et al.,2015；Rolfe et al.,2016
PbGH3	修饰生长素和茉莉酸 Modify auxin and jasmonic acid	Schwelm et al.,2015
PbCYP3	可能通过参与调控宿主植物的油菜素内酯信号通路，促进感染过程。在Magnaporthe oryzae突变体中异源表达恢复了毒力 Manipulates the host dependency to promote brassinosteroid levels possibly. Heterologous expression of PbCYP3 in Magnaporthe oryzae mutantΔCyp1 increase virulence	Singh et al.,2018
PbRING1	具有功能性信号肽和 E3泛素连接酶活性 Harbors a functional N-terminal signal peptide and displays the E3 ligase activity	Yu et al.,2019
G-protein-coupled receptors (GPCR) signal pathway	从根肿菌菌株ZJ-1中鉴定了多个GPCR通路相关基因，可能参与感知和识别来自寄主的外部信号 GPCR pathway-related genes were identified in P. brassicae ZJ-1，involved in the perception and recognition of external signals of the host	Bi et al.,2019
SSPbP22	体外试验证实其具有激酶活性 Has kinase activity	Pérez-López et al.,2020
SSPbP53	半胱氨酸蛋白酶抑制剂 Inhibits cruciferous papain-like cysteine proteases	Pérez-López et al.,2020,2021
PBZF1	与SnRK1.1互作，抑制其功能，增强病原菌致病力 Interacts with SnRK1.1 to inhibite the biological function of SnRK1.1 and promotes the virulence of P. brassicae	Chen et al.,2021
indole-3-acetaldehyde dehydrogenase	与IAA合成相关 Indole acetic acid synthesis	Galindo-González et al.,2021
PbPE13	鉴定到的PbPEs可调控PTI反应 Triggers PAMP immune response	Hossain et al.,2021
PbChiB2/ PbChiB4	甘油几丁质结合域CBM18可结合几丁质和休眠孢子，抑制几丁质触发的免疫反应 Binds to spores and to chitin oligomers，suppressing chitin-triggered immunity during infection	Muirhead & Perez-Lopez,2022
Pb4_102097/Pb4_108104	诱导细胞死亡，促进过氧化氢积累 Induces cell death and are associated with H₂O₂ accumulation	Zhan et al.,2022
PbE3-2	RING型E3泛素连接酶，抑制植物免疫反应 A RING-type E3 ubiquitin ligases and impedes host immunity	Li et al.,2024
PbHMWSP34	抑制JA、ET、SA信号途径相关基因表达 Inhibits the expression of JA，ET，and several SA signaling pathway genes	Feng et al.,2024
PbZFE1	转录因子型效应因子，诱导宿主细胞异常分裂和细胞伸长 A transcription factor-type effector during pathogenesis，inducing abnormal cell division and cell elongation in the host	Ando et al.,2024
Pb257	诱导细胞死亡，促进根部肿大Triggers cell death	Yang et al.,2024
PbPE23	含有丝氨酸/苏氨酸激酶结构域，异源表达证实其诱导坏死。其在初级侵染到次级侵染过渡时高表达 Contains a serine/threonine kinase domain and induces necrosis after heterologous expression high expression at the transition stages from primary to secondary infection	Hossain et al.,2025

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寄主Host	Pb1	Pb2	Pb3	Pb4	Pb5	Pb6	Pb7	Pb8	Pb9	Pb10	Pb11	Pb12	Pb13	Pb14	Pb15	Pb16
H01	-	-	-	-	-	-	-	-	-	+	-	-	-	-	-	-
H02	-	-	-	-	-	-	-	-	+	+	+	-	-	+	+	+
H03	-	-	-	-	-	-	+	+	+	+	+	-	-	-	+	-
H04	-	-	-	-	-	+	-	+	+	+	+	-	+	-	+	+
H05	-	-	-	+	+	+	-	+	-	-	+	-	-	+	+	+
H06	-	-	-	+	-	-	-	-	-	-	+	+	-	+	-	+
H07	-	-	+	-	-	-	-	-	-	-	-	-	+	-	-	-
H08	-	+	-	-	-	-	-	-	-	-	-	-	-	-	-	-
H09	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+

寄主Host	Pb1	Pb2	Pb3	Pb4	Pb5	Pb6	Pb7	Pb8	Pb9	Pb10	Pb11	Pb12	Pb13	Pb14	Pb15	Pb16
H01	-	-	-	-	-	-	-	-	-	+	-	-	-	-	-	-
H02	-	-	-	-	-	-	-	-	+	+	+	-	-	+	+	+
H03	-	-	-	-	-	-	+	+	+	+	+	-	-	-	+	-
H04	-	-	-	-	-	+	-	+	+	+	+	-	+	-	+	+
H05	-	-	-	+	+	+	-	+	-	-	+	-	-	+	+	+
H06	-	-	-	+	-	-	-	-	-	-	+	+	-	+	-	+
H07	-	-	+	-	-	-	-	-	-	-	-	-	+	-	-	-
H08	-	+	-	-	-	-	-	-	-	-	-	-	-	-	-	-
H09	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+

寄主Host	Pb1	Pb2	Pb3	Pb4	Pb5	Pb6	Pb7	Pb8	Pb9	Pb10	Pb11	Pb12	Pb13	Pb14	Pb15	Pb16
H01	-	-	-	-	-	-	-	-	-	+	-	-	-	-	-	-
H02	-	-	-	-	-	-	-	-	+	+	+	-	-	+	+	+
H03	-	-	-	-	-	-	+	+	+	+	+	-	-	-	+	-
H04	-	-	-	-	-	+	-	+	+	+	+	-	+	-	+	+
H05	-	-	-	+	+	+	-	+	-	-	+	-	-	+	+	+
H06	-	-	-	+	-	-	-	-	-	-	+	+	-	+	-	+
H07	-	-	+	-	-	-	-	-	-	-	-	-	+	-	-	-
H08	-	+	-	-	-	-	-	-	-	-	-	-	-	-	-	-
H09	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+

寄主Host	Pb1	Pb2	Pb3	Pb4	Pb5	Pb6	Pb7	Pb8	Pb9	Pb10	Pb11	Pb12	Pb13	Pb14	Pb15	Pb16
H01	-	-	-	-	-	-	-	-	-	+	-	-	-	-	-	-
H02	-	-	-	-	-	-	-	-	+	+	+	-	-	+	+	+
H03	-	-	-	-	-	-	+	+	+	+	+	-	-	-	+	-
H04	-	-	-	-	-	+	-	+	+	+	+	-	+	-	+	+
H05	-	-	-	+	+	+	-	+	-	-	+	-	-	+	+	+
H06	-	-	-	+	-	-	-	-	-	-	+	+	-	+	-	+
H07	-	-	+	-	-	-	-	-	-	-	-	-	+	-	-	-
H08	-	+	-	-	-	-	-	-	-	-	-	-	-	-	-	-
H09	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+	+