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作物学报 ›› 2022, Vol. 48 ›› Issue (6): 1372-1388.doi: 10.3724/SP.J.1006.2022.12031

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

基于Meta-QTL和RNA-seq的整合分析挖掘水稻抗稻瘟病候选基因

田甜(), 陈丽娟, 何华勤*()   

  1. 福建农林大学生命科学学院, 福建福州 350002
  • 收稿日期:2021-04-28 接受日期:2021-10-19 出版日期:2022-06-12 网络出版日期:2021-11-12
  • 通讯作者: 何华勤
  • 作者简介:E-mail: Tiantian_hbfzcs@126.com
  • 基金资助:
    国家自然科学基金项目(81502091)

Identification of rice blast resistance candidate genes based on integrating Meta-QTL and RNA-seq analysis

TIAN Tian(), CHEN Li-Juan, HE Hua-Qin*()   

  1. College of Life Science, Fujian Agriculture and Forestry University, Fuzhou 350002, Fujian, China
  • Received:2021-04-28 Accepted:2021-10-19 Published:2022-06-12 Published online:2021-11-12
  • Contact: HE Hua-Qin
  • Supported by:
    National Natural Science Foundation of China(81502091)

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摘要：

稻瘟病菌严重威胁水稻生产, 且稻瘟病菌变异快导致抗稻瘟病品种在短短数年后就失去抗性。因此, 不断挖掘新的抗稻瘟病基因对培育具有广谱抗病品种至关重要。本研究对43篇文献的783个抗稻瘟病QTL进行元分析, 在12条染色体上鉴定到50个Meta-QTL (至少有2个原始QTL映射), 平均区间距离为0.87 Mb, 共计包含4718个区间基因。随后将抗稻瘟病Meta-QTL和RNA-seq进行整合分析, 结果鉴定出2193个既定位于抗稻瘟病Meta-QTL区间上, 又响应稻瘟病胁迫的显著差异表达的共同基因, 其中22个基因已经克隆且被报道与水稻抗稻瘟病等逆境防御过程相关。此外, 从上述共同基因中筛选出99个抗性基因类似物(resistance gene analogue, RGA)和112个转录因子(transcription factor, TF), 对这些基因构建基因共表达网络图, 基于连接度前20筛选出网络图的hub基因, 其中OsJAMyb、bsr-d1和OsWRKY76已被报道与水稻抗稻瘟病相关, 而OsSPL9参与水稻抗条纹病毒调控通路中, 剩余hub基因作为重要的潜在抗性基因, 有待进一步功能验证, 为培育广谱抗性的水稻品种奠定基础。

关键词: 水稻, 抗稻瘟病, 元分析, RNA-seq, 候选基因

Abstract:

Magnaporthe oryzae seriously devastates rice production, and resistant cultivars can lose resistance within a few years due to the pathogenic variability of M. oryzae. Therefore, it is essential to explore continuously novel blast-resistance genes for breeding broad-spectrum resistance cultivars. In this study, firstly, 50 Meta-QTLs (including at least 2 original QTLs) were identified on 12 chromosomes by meta-analysis of blast-resistance 783 QTLs from 43 literatures. The average interval distance was 0.87 Mb in these Meta-QTLs, which contained a total of 4718 interval genes. Subsequently, based on integrated analysis of blast-resistance Meta-QTLs and RNA-seq, the result identified 2193 common genes which were not only located on blast-resistance Meta-QTLs, but also significantly differentially expressed in response to the M. oryzae. Among them, 22 cloned genes had been reported to be involved in defense responses to M. oryzae and other stresses. Furthermore, 99 resistance gene analogues (RGA) and 112 transcription factors (TF) were screened out from the above common genes, which were utilized to construct gene co-expression networks (GCEN). Based on the Top 20 of the connection degrees, hub genes were identified in the GCEN. Among them, OsJAMyb, bsr-d1, and OsWRKY76 had been reported to be against rice blast, and OsSPL9 was related to resistance to rice stripe virus. The left hub genes were considered as important potential resistance genes which need further functional verification to prepare for breeding broad-spectrum resistance rice cultivars.

Key words: rice (Oryza sativa L.), blast resistance, meta-analysis, RNA-seq, candidate gene

表1

水稻抗稻瘟病QTL信息汇总"

作图群体
Population		 群体类型
Population type		 群体大小
Number of population		 作图方法
Mapping method		 QTL数目
Number of QTLs		 参考文献
Reference
Moreberekan×Co39 RILs 281 IM 22 Wang et al., 1994[28]
IR64×Azucena DH 114 IM 13 Bagali et al., 2000[4]
Nipponbare×Owarihatamochi F2 146 IM 4 Fukuoka et al., 2001[29]
Zhong 156×Gumei 2 RILs 146 CIM 2 Fan et al., 2001[30]
Kahei×Koshihikari F2 241 SMA 2 Miyamoto et al., 2001[31]
Khao Dawk Mali 105×CT9993 RILs 141 SIM, CIM 6 Sirithunya et al., 2002[32]
Lemont×Teqing RILs 284 IM 11 Tabien et al., 2002[33]
Norin 29×Chubu 32 F2 149 IM 1 Zenbayashi et al., 2002[34]
Lemont×Teqing RILs 292 IM 14 Loan et al., 2003[35]
Zhenshan 97×Minghui 63 RILs 241 CIM 12 Chen et al., 2003[36]
IR64×Azucena DH 105 CIM 9 Sallaud et al., 2003[37]
Bala×Azucena RILs 205 CIM 29 Talukder et al., 2004[38]
Bala×Azucena RILs 100 CIM 12 Talukder et al., 2005[39]
ZYQ8×JX17 DH 127 SMA 77 Xu et al., 2004[40]
Zhong 156×Gumei 2 RILs 304 MIM 21 Wu et al., 2005[6]
URN12×Koshihikari F2 136 IM 2 Sato et al., 2006[41]
作图群体
Population		 群体类型
Population type		 群体大小
Number of population		 作图方法
Mapping method		 QTL数目
Number of QTLs		 参考文献
Reference
Llanos 5×Fanny RILs 120 IM, CIM 37 Lopez et al., 2006[42]
KDML105×JHN RILs 587 SIM, sCIM 14 Noenplab et al., 2006[43]
Bala×Azucena Nd No CIM 83 Ballini et al., 2008[44]
Suweon 365×Chucheong RILs 190 CIM 54 Cho et al., 2008[45]
Heikezijing×Suyunuo RILs 166 CIM 44 Shi et al., 2010[46]
IR64×Azucena DH 111 CIM 4 Kongprakhon et al., 2010[47]
Lemont×Jasmine 85 RILs 227 CIM 9 Jia et al., 2011[48]
Way Rarem×Oryzica Llanos 5 BILs 123 IM 16 Lestari et al., 2011[49]
TAM×KHZ F2:3 192 CIM 7 Sabouri et al., 2011[50]
IR68835×KDML105 BILs 83 SMA 19 Korinsak et al., 2011[51]
TY×CO39 RILs 363 CIM 22 Wang et al., 2012[52]
MR219×IRGC105491 BILs 261 CIM 9 Rahim et al., 2012[53]
BILs 63 13
MWG×EW8 DH 96 CIM 3 Yang et al., 2012[54]
Pongsu seribu 2×Mahsuri F3 296 IM, CIM 40 Ashkani et al., 2013a[55]
Pongsu seribu 2×Mahsuri F3 188 SMA, IM, CIM 13 Ashkani et al., 2013b[56]
Bodao×Suyunuo RILs 155 CIM 13 Huan et al., 2014[57]
IT×Koshihikari F3 124 CIM 1 Mizobuchi et al., 2014[58]
R287×Ximaxian BILs 299 CIM 29 Liu et al., 2015[59]
GV×VN F2 114 SIM 2 Urso et al., 2016[5]
landraces Landraces 276 SMA 31 Wu et al., 2016[60]
Heikezijing×Suyunuo RILs 162 ICIM 2 Fang et al., 2016[61]
Danteshwari×Dagaddeshi RILs 122 CIM 14 Mandal et al., 2017[62]
Nekken 2×Hokuriku 193 F3 243 CIM 9 Nagaoka et al., 2017[63]
Heikezijing×Suyunuo RILs 162 ICIM 5 He et al., 2017[64]
Cybonnet×Saber RILs 243 ICIM 22 Chen et al., 2018[65]
Bodao×Suyunuo RILs 212 ICIM 2 Fang et al., 2019[66]
Jin 23B×CR071 BILs 239 CIM 16 Jiang et al., 2020[67]
Jin 23B×Qinggu'ai 3 237 13

图1

水稻抗稻瘟病的“一致性”QTL图谱和元分析结果 标尺刻度为物理图距(mega base, Mb); 柱状体代表染色体, 染色体右侧为分子标记及其具体物理位置; 分子标记右侧竖线为映射到“一致性”图谱上的原始QTL; 染色体上的蓝色片段代表Meta-QTL。"

表2

水稻抗稻瘟病QTL的元分析"

Meta-QTL 染色体
Chr.		 侧翼标记
Flanking markers		 置信区间
95% CI (Mb)		 图距
Map distance (Mb)		 原始QTL
Original QTLs		 区间基因
Interval gene		 已报道的抗稻瘟病基因
Published blast-resistance gene
Metaq1-2 1 UMC32-RM243 7.34-7.97 0.63 3 89 Pi27(t)[68]
Metaq1-4 1 OSR3-C2340 34.03-34.47 0.44 3 51
Metaq2-1 2 C149-RM174 5.91-7.01 1.10 3 143
Metaq2-2 2 RG25-RZ401 21.77-24.047 2.28 4 295
Metaq2-3 2 RZ58-RM6 28.69-29.58 0.89 2 124
Metaq2-5 2 RM482-RZ213 35.27-35.37 0.10 2 20 Pi25(t)[37], Pi-tq5[69], Pi-b[70]
Metaq3-1 3 RM1332-RG409 2.45-3.50 1.04 2 182
Metaq3-2 3 RM1338-RM232 8.39-9.76 1.37 2 210
Metaq3-3 3 RM15080-RM15111 15.40-15.69 0.30 2 41
Metaq3-4 3 RM411-RM487 21.43-22.02 0.59 4 52
Metaq3-5 3 RM5626-ud3001344 24.86-25.04 0.18 7 15
Metaq4-1 4 RM1359-G271 19.86-20.17 0.31 6 48
Metaq4-2 4 RM1136-CT206 25.04-25.36 0.32 5 16
Metaq4-4 4 G264-RG214 31.34-31.66 0.32 5 51 Pi39(t)[71], Pi46(t)[72]
Metaq4-5 4 RM124-RM280 34.74-34.99 0.25 2 34
Metaq5-1 5 RM122-RM2010 0.31-0.49 0.18 3 132
Metaq5-2 5 RM574-RM437 3.45-3.88 0.43 3 51
Metaq5-3 5 wd5001198-wd5001344 10.36-10.86 0.50 2 13
Metaq5-4 5 R2289-RM161 18.96-20.90 1.95 2 220
Metaq5-5 5 C43-RM3476 22.26-23.91 1.64 7 229
Metaq6-1 6 RZ2-C226A 3.36-3.54 0.17 3 24
Metaq6-2 6 RZ144-RZ667 6.72-6.93 0.21 6 30
Metaq6-3 6 RM19779-RM527 9.31-9.86 0.55 9 30 Pi40(t)[73], Pi26[6], Pi59(t)[74]
Metaq6-6 6 RZ242-RG653 28.96-29.03 0.06 4 15 Pi-tq1[69]
Metaq7-1 7 ud7000014-RG773 0.31-4.05 3.74 2 458
Metaq7-2 7 RM180-L538T7 5.74-7.74 2.00 5 158
Metaq7-3 7 RM5481-RM11 16.20-19.26 3.06 4 225
Metaq7-4 7 RM182-RZ626 21.51-23.11 1.60 4 208
Metaq7-5 7 R1789-C507 26.53-26.71 0.18 8 26
Metaq8-1 8 RM25-ud8000289 4.38-4.65 0.27 2 34
Metaq8-2 8 RM310-RM547 5.12-5.59 0.48 9 67 Pi42(t)[75]
Metaq8-3 8 ud8000924-RM44 14.78-16.57 1.79 6 89
Metaq8-4 8 RM7049-ud8001357 20.81-21.03 0.21 9 24
Metaq9-1 9 R1687-C1454 8.35-9.63 1.28 4 62 Pi15[76]
Metaq9-2 9 R1751-RM434 14.36-15.66 1.30 5 154
Metaq9-3 9 RM108-CT6 19.30-20.17 0.87 5 150
Metaq9-4 9 RM1553-RM24777 21.00-22.05 1.04 10 168
Metaq10-1 10 RM7217-R2174 4.64-5.50 0.86 5 53
Metaq10-2 10 G1125-RM8207 7.35-9.81 2.46 2 114
Meta-QTL 染色体
Chr.		 侧翼标记
Flanking markers		 置信区间
95% CI (Mb)		 图距
Map distance (Mb)		 原始QTL
Original QTLs		 区间基因
Interval gene		 已报道的抗稻瘟病基因
Published blast-resistance gene
Metaq10-5 10 RG561-RM228 21.78-22.24 0.47 2 95
Metaq11-1 11 RM26198-RM552 4.42-4.84 0.42 7 36
Metaq11-4 11 RM6680-RM2596 18.62-19.97 1.35 5 110 Pi38[77], Pi34[78], Pi7(t)[28],
Metaq11-5 11 RM27088-RM2191 23.77-24.66 0.89 4 73 Pi47[79]
Metaq11-6 11 RM224-L190 27.67-28.24 0.56 9 49 Pik[80], Pik-p[81], Pi44(t)[82], Pi-1(t)[83], Pi1[84], Pik-m[85], Pi49[86], Pi-hk1[87], Pi43(t)[75]
Metaq12-1 12 RZ816-RM491 2.43-3.58 1.16 6 143
Metaq12-2 12 G1391-ud12000339 5.81-6.14 0.33 4 14 Pi-tq6[69], Pi6(t)[88]
Metaq12-3 12 RM101-ud12000566 8.83-9.23 0.40 4 16
Metaq12-4 12 C625-ud12000700 11.06-11.32 0.26 13 23 Pi-42(t)[75], Pi58(t)[74]
Metaq12-5 12 RM27982-RM7102 12.63-13.21 0.58 3 27 Pi48[79]
Metaq12-6 12 RM309-RM3326 21.45-21.74 0.29 9 27

图2

在Guy11稻瘟病菌胁迫下水稻抗病品种Pi_gm的差异表达基因的火山图"

图3

水稻抗稻瘟病Meta-QTL和RNA-seq的整合分析结果 A: 水稻抗稻瘟病Meta-QTL和RNA-seq的共同基因; B: 水稻抗稻瘟病Meta-QTL和RNA-seq的共同RGA基因的类型; C: 水稻抗稻瘟病Meta-QTL和RNA-seq的共同基因的TF基因的类型。"

图4

响应稻瘟病胁迫表达的RGA和TF的共表达网络图 A: 响应稻瘟病胁迫表达上调的RGA和TF的共表达网络图; B: 响应稻瘟病胁迫表达下调的RGA和TF的共表达网络图。图中球形表示为抗性基因类似物(RGA), 箭头形表示为转录因子(TF), 不同颜色代表不同的degree值, 从绿色到红色代表连接度(connection degree)从小到大, 颜色越红, 代表该基因在网络图的连接作用越大。"

表3

在上调基因共表达网络中连接度前20的hub基因"

Meta-QTL Degree值
Degree score		 基因ID
Gene ID		 基因符号
Gene symbol		 表达倍数
log2(Fold Change)		 功能注释
Function annotation
Metaq2-3 73 Os02g0700300 OsDLN66 10.04 MYB family transcription factor
Metaq9-2 73 Os09g0417600 OsWRKY76 9.10 WRKY76
Metaq3-4 73 Os03g0437200 bsr-d1 8.88 ZOS3-12-C2H2 zinc finger protein
Metaq5-4 73 Os05g0418800 NAC87 8.23 No apical meristem protein
Metaq5-1 73 Os05g0121600 RSR1 8.14 AP2 domain containing protein
Meta-QTL Degree值
Degree score		 基因ID
Gene ID		 基因符号
Gene symbol		 表达倍数
log2(Fold Change)		 功能注释
Function annotation
Metaq11-6 73 Os11g0686250 OsWRKY41 8.11 WRKY63
Metaq11-6 73 Os11g0684000 OsJAMyb 7.54 MYB family transcription factor
Metaq8-1 73 Os08g0179400 OsbHLH070 7.49 Expressed protein
Metaq2-2 73 Os02g0603600 OsbHLH110 5.58 Helix-loop-helix DNA-binding domain containing protein
Metaq5-4 73 Os05g0421600 OsNAC52 5.27 No apical meristem protein
Metaq11-6 73 Os11g0685700 OsWRKY61 4.67 WRKY61
Metaq2-2 73 Os02g0606200 OsBBX4 4.62 B-box zinc finger family protein
Metaq7-1 73 Os07g0111400 OsWRKY29 4.57 WRKY29
Metaq2-1 73 Os02g0221100 OsbHLH029 4.29 Helix-loop-helix DNA-binding domain containing protein
Metaq7-1 73 Os07g0119300 — 4.09 MYB family transcription factor
Metaq2-2 73 Os02g0610500 OsCOL4 3.56 CCT/B-box zinc finger protein
Metaq1-2 73 Os01g0236700 OsNLP3 3.46 NIN
Metaq7-4 73 Os07g0568300 OsTZF6 2.68 Zinc finger family protein
Metaq7-3 73 Os07g0484700 — 2.07 MYB family transcription factor
Metaq5-4 73 Os05g0408200 OsSPL9 1.94 OsSPL9-SBP-box gene family member

表4

在下调基因共表达网络中连接度前20的hub基因"

Meta-QTL Degree值
Degree score		 基因ID
Gene ID		 基因符号
Gene symbol		 表达倍数
log2(Fold Change)		 功能注释
Function annotation
Metaq9-1 56 Os09g0326100 — -6.34 Receptor-like protein kinase 5 precursor
Metaq7-1 56 Os07g0106000 — -2.85 Ser/thr protein phosphatase family protein
Metaq12-1 56 Os12g0149700 — -4.77 Protein kinase
Metaq7-2 55 Os07g0211400 OsKAPP -1.54 Protein kinase-associated protein phosphatase
Metaq10-5 55 Os10g0561500 OsRLCK307 -1.89 Protein kinase family protein
Metaq7-1 55 Os07g0116900 — -1.71 NB-ARC domain containing protein
Metaq5-4 55 Os05g0406800 — -3.82 Receptor-like protein kinase precursor
Meta-QTL Degree值
Degree score		 基因ID
Gene ID		 基因符号
Gene symbol		 表达倍数
log2(Fold Change)		 功能注释
Function annotation
Metaq4-5 55 Os04g0685900 OsRLCK174 -1.88 Receptor protein kinase TMK1 precursor
Metaq5-5 55 Os05g0478300 — -5.79 Receptor-like protein kinase 2 precursor
Metaq7-1 55 Os07g0134200 OsRLCK222 -3.21 Receptor protein kinase CLAVATA1 precursor
Metaq5-5 55 Os05g0467000 OsCDPK16 -2.41 CAMK_CAMK_like.29-CAMK includes calcium/ calmodulin dependent protein kinases
Metaq5-5 55 Os05g0480400 — -1.89 Inactive receptor kinase At2g26730 precursor
Metaq2-1 55 Os02g0215900 OsGIRL1 -3.52 Receptor kinase
Metaq7-3 55 Os07g0501800 — -4.16 Leucine-rich repeat family protein
Metaq6-1 55 Os06g0170100 OsWAK63 -8.85 OsWAK63-OsWAK receptor-like protein kinase
Metaq7-1 55 Os07g0145400 OsGHR1 -10.94 Leucine-rich repeat family protein
Metaq7-5 55 Os07g0641200 OsCDPK30 -3.12 CAMK_CAMK_like.36-CAMK includes calcium/ calmodulin depedent protein kinases
Metaq5-5 55 Os05g0466900 — -1.91 Protein kinase family protein
Metaq4-2 55 Os04g0506100 — -2.90 Receptor-like protein kinase precursor
Metaq2-1 54 Os02g0212900 OsRLCK66 -2.77 Cysteine-rich receptor-like protein kinase 35 precursor

表5

22个已克隆且与抗稻瘟病相关的基因"

Meta-QTL 基因ID
Gene IDs		 已公布的基因
Published genes		 表达倍数
log2(Fold Change)		 差异表达
Differential exprssion		 抵御胁迫
Resistance to stress
Metaq3-1 Os03g0160100 OsEDR1 2.29 上调Up-regulation Blast[101]; Xoo[95]
Metaq3-2 Os03g0277000 OsGDI3 2.19 上调Up-regulation Disease resistance[102,103]
Metaq3-3 Os03g0390200 OsSAPK1 3.01 上调Up-regulation Xoo[104]
Metaq3-4 Os03g0437200 Bsr-d1 8.88 上调Up-regulation Blast[97]
Metaq5-1 Os05g0110900 OsRLCK176 1.90 上调Up-regulation Xoo[105]; Chitin[106]
Metaq5-4 Os05g0408200 OsSPL9 1.94 上调Up-regulation RDV[100]
Metaq7-1 Os07g0129200 OsPR1a 6.48 上调Up-regulation Pathogen infection[107]
Metaq7-2 Os07g0217600 CYP71Z2 14.17 上调Up-regulation Xoo[108]
Metaq7-3 Os07g0471300 OsAGO18 3.43 上调Up-regulation Virus[109]
Metaq7-3 Os07g0492000 OsNDPK1 2.42 上调Up-regulation Bacterial pathogens[110]
Metaq7-3 Os07g0500300 OsGAP 3.55 上调Up-regulation ABA[111]
Metaq7-4 Os07g0545800 CIGR1 1.56 上调Up-regulation Blast and gibberellin[112]
Metaq7-4 Os07g0569100 OsREM4.1 2.22 上调Up-regulation ABA[113]
Metaq9-2 Os09g0417600 OsWRKY76 9.10 上调Up-regulation Blast[99]
Metaq9-2 Os09g0417800 OsWRKY62 9.46 上调Up-regulation Xoo[114]
Metaq10-5 Os10g0564500 OsSAPK3 4.85 上调Up-regulation Xoo[104]
Metaq11-1 Os11g0195500 OsPAD4 2.02 上调Up-regulation Xoo[115]
Metaq11-6 Os11g0684000 OsJAMyb 7.54 上调Up-regulation Blast[98]
Metaq5-1 Os05g0111300 OsMT2b -4.24 下调Down-regulation ROS[116]
Metaq7-1 Os07g0152000 OsTCP21 -1.92 下调Down-regulation RRSV[117]
Metaq9-3 Os09g0513000 OsBIANK1 -2.12 下调Down-regulation Blast[118]
Metaq9-4 Os09g0544800 OsRacGEF1 -3.50 下调Down-regulation Blast[25]
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