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Acta Agronomica Sinica ›› 2024, Vol. 50 ›› Issue (4): 820-835.doi: 10.3724/SP.J.1006.2024.34144

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Identification of candidate genes associated with drought tolerance based on QTL and transcriptome sequencing in Brassica napus L.

LI Yang-Yang1,2,3(), WU Dan2,3, XU Jun-Hong2,3, CHEN Zhuo-Yong1,2,3, XU Xin-Yuan1,2,3, XU Jin-Pan1,2,3, TANG Zhong-Lin1,2,3, ZHANG Ya-Ru1,2,3, ZHU Li1,2,3, YAN Zhuo-Li1,2,3, ZHOU Qing-Yuan1,2,3, LI Jia-Na1,2,3, LIU Lie-Zhao1,2,3, TANG Zhang-Lin1,2,3,*()   

  1. 1Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, Chongqing 401329, China
    2College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China
    3Academy of Agricultural Sciences, Southwest University, Chongqing 400715, China
  • Received:2023-08-24 Accepted:2023-10-23 Online:2024-04-12 Published:2023-11-13
  • Contact: * E-mail: tangzhlin@swu.edu.cn
  • Supported by:
    National Key Research and Development Program of China(2022YFD1201600);Chongqing Technology Innovation and Application Development Key Project(cstc2021jscx-cylhX0003)

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Abstract:

Drought stress severely limits planting promotion and yield increase in Brassica napus L. Drought tolerance is a complex quantitative trait controlled by multiple genes. Combining QTL and transcriptome is an effective method for identifying candidate genes associated with drought tolerance in B. napus. In this study, the seedlings of F2:6 and F2:8 recombinant inbred lines, constructed by Sanliu’ai (drought sensitivity line) and Kelina-2 (drought tolerance line), were treated with drought stress and well watering at seedling stage. Shoot fresh weight, shoot dry weight, leaf relative water content, malondialdehyde content, and soluble sugar content were measured. The QTL and candidate intervals were identified based on genetic linkage maps, which were constructed using SSR and SNP markers with polymorphism. Subsequently, candidate genes associated with drought tolerance were screened by combining transcriptome sequencing of No11 (drought tolerance material) and No28 (drought sensitivity material). Drought stress decreased shoot fresh weight, shoot dry weight, and leaf relative water content, and increased the contents of malondialdehyde and soluble sugar. QTL and candidate intervals related to drought tolerance were distributed on chromosome A01, A02, A06, A08, A09, A10, C02, C03, C04, C06, and C09. By transcriptome analysis of drought tolerance and sensitivity materials under well water, drought stress for 24, 36, and 48 h, the major different expression genes were enriched in the pathways associated with photosynthesis, fatty acid metabolism, amino acid metabolism, plant hormone signal transduction, ribosome, circadian rhythm and biosynthesis of keratin, cork and wax. A total of 28 candidate genes related to drought tolerance were identified by combining QTL and transcriptome. They coded FLC, bHLH105, TGA4, TEM1, ERF003, ACO3, CHLI1, LHCB6, PORC, etc., which had transcription factor activity, ethylene production and signal transduction, chlorophyll biosynthesis and binding, chlorophyll oxidoreductase and encoding ribosome proteins. These results could provide a basis for revealing drought tolerance mechanism and molecular breeding of drought tolerance variety in B. napus.

Key words: Brassica napus L., drought tolerance, QTL, transcriptome, candidate genes

Table 1

Variance analysis of traits relation to drought tolerance in rapeseed F2:6 and F2:8 RIL populations"

群体
Population		 变异来源
Source of variation		 RWC SFW SDW SUG MDA
DF F-value DF F-value DF F-value DF F-value DF F-value
F2:6 水分间Water 1 11.18** 1 850.03** 1 214.32** 1 30.86** 1 91.75**
家系间Line 103 4.64** 104 14.41** 104 14.96** 104 15.29** 104 552.39**
水分×家系
Water×Line		 103
 3.10**
 104
 10.55**
 104
 5.98**
 104
 9.96**
 104
 392.10**
误差Error 208 210 210 210 210
F2:8 水分间Water 1 3175.43** 1 2237.27** 1 389.89** 1 1490.35** 1 1139.48**
家系间Line 125 2.36** 125 6.25** 125 6.21** 125 15.72** 125 21.62**
水分×家系
Water×Line		 125
 2.30**
 124
 3.65**
 124
 1.76**
 124
 13.32**
 123
 11.86**
误差Error 446 426 414 462 471

Table 2

Descriptive statistics of traits relation to drought tolerance in rapeseed parental, F2:6 and F2:8 RIL populations"

性状
Trait		 群体
Population		 处理
Treatment		 亲本Parent 群体Population
三六矮
Sanliu’ai		 科里纳-2
Kelina-2		 平均值
Average		 标准误差
SE		 变幅
Range		 峰度
Kurtosis		 偏度
Skewness
RWC (%) F2:6 CK 91.72 93.35 86.51 0.54 68.96-96.55 0.95 -0.76
DS 83.98 86.24 85.16 0.58 61.78-96.87 2.27 -1.19
F2:8 CK 88.00 86.84 89.74 0.28 72.10-95.14 7.26 -1.64
DS 65.46 76.11 71.27 0.42 60.83-82.91 -0.55 -0.06
SFW (g) F2:6 CK 20.18 10.78 16.55 0.46 4.79-30.27 0.01 0.21
DS 15.67 9.00 11.71 0.36 4.79-23.90 0.15 0.71
F2:8 CK 44.78 27.06 36.79 1.02 11.84-75.42 1.57 1.04
DS 19.22 22.70 14.36 0.38 6.58-25.85 -0.03 0.62
SDW (g) F2:6 CK 1.27 0.72 1.18 0.04 0.41-2.34 0.06 0.64
DS 0.95 0.61 0.95 0.03 0.37-1.92 0.47 0.87
F2:8 CK 3.80 2.65 2.72 0.08 0.89-5.90 0.85 0.74
DS 2.30 2.10 1.81 0.05 0.59-3.48 0.90 0.59
SUG (μg g-1) F2:6 CK 1496.20 542.03 2744.17 226.85 186.82-16219.47 12.23 2.83
DS 6485.20 1081.01 3271.71 249.66 222.49-12447.88 3.50 1.69
F2:8 CK 3888.00 4581.34 5349.75 131.73 2144.61-10444.09 0.82 0.75
DS 6265.26 7643.01 7278.97 131.53 3370.63-10742.93 0.17 0.15
MDA (μmol g-1) F2:6 CK 7.49 13.97 9.80 0.44 3.43-34.67 8.58 2.26
DS 12.77 17.70 10.04 0.34 5.28-23.09 1.81 1.31
F2:8 CK 41.18 20.43 29.26 0.97 9.34-64.77 0.54 0.83
DS 50.15 50.63 41.03 1.04 23.76-71.73 -0.63 0.51

Fig. 1

Distribution of traits relation to drought tolerance in rapeseed F2:6 and F2:8 RIL populations Abbreviations are the same as those given in Tables 1 and 2."

Fig. 2

Traits associated with drought tolerance in drought resistance and sensitivity rapeseed **: P < 0.01. Abbreviations are the same as those given in Table 1."

Fig. 3

Genetic linkage map based on SSR and QTL distribution DRI: drought resistance index. The other abbreviations are the same as those given in Tables 1 and 2."

Fig. 4

Genetic linkage map based on SNP and QTL distribution"

Table 3

QTL and candidate range of traits associated with drought tolerance in rapeseed"

群体
Population		 QTL 置信区间
Confidence interval (cM)		 邻近标记
Marker		 物理位置
Physical position
(bp)		 阈值
LOD		 染色体
Chr.		 候选区间
Candidate range
(bp)
F2:6 qSFWCK-A01 78.85-86.82 AX-95683221 4227188 3.04 A01 4047188-4407188
AX-179306831 4399498 2.89 A01 4219498-4579498
F2:8 qRWCDRI-A02 17.64-31.87 AX-177910459 262823 3.07 A02 82823-442823
F2:8 qRWCDS-A02 16.64-33.30 AX-177910459 262823 2.99 A02 82823-442823
F2:8 qSFWCK-A02 43.41-47.22 AX-177829332 4692035 2.53 A02 4512035-4872035
F2:8 qSUGCK-A02 0.00-8.00 AX-177834286 20489037 3.20 A02 20309037-20669037
F2:6 qSDWCK-A02 0.00-11.74 SWUA02_198 893419-893684 3.14 A02 713419-1073684
A02_2 893423-893813 3.47 A02 713423-1073813
F2:8 qSFWDRI-A06 136.38-140.39 AX-95506320 20609909 2.50 A06 20429909-20789909
F2:8 qMDACK-A08 28.40-30.85 AX-95638560 11831251 2.58 A08 11331251-12331251
F2:8 qSFWDRI-A08 89.56-109.10 AX-95637797 16969405 3.04 A08 16469405-17469405
F2:6 qSDWCK-A09 37.27-44.43 AX-179306992 2292222 2.59 A09 1912222-2672222
F2:6 qSFWCK-A09 37.27-44.43 AX-179306992 2292222 2.70 A09 1912222-2672222
F2:8 qMDADRI-A09 163.36-165.01 AX-177830392 26135201 4.09 A09 25755201-26515201
F2:6 qMDACK-A09 0.00-2.00 nia_m046 21769576-21769946 2.91 A09 21389576-22149946
F2:6 qRWCDS-A09 0.00-2.00 nia_m046 21769576-21769946 2.87 A09 21389576-22149946
F2:8 qRWCCK-A10 12.22-14.56 AX-182144456 885133 3.06 A10 675133-1095133
F2:6 qSFWDRI-A10 134.63-148.54 AX-177911667 16025485 3.04 A10 15815485-16235485
AX-95637504 16164216 3.08 A10 15954216-16374216
AX-182169619 16167478 3.04 A10 15957478-16377478
F2:8 qSUGCK-C02 7.00-45.13 AX-182158861 16526368 2.58 C02 15326368-17726368
AX-95636960 16803922 3.01 C02 15603922-18003922
AX-182136799 24120437 2.99 C02 22920437-25320437
AX-182139036 28872169 3.49 C02 27672169-30072169
AX-182125192 33288173 2.98 C02 32088173-34488173
AX-105306912 34988363 2.58 C02 33788363-36188363
AX-95505280 41712868 2.96 C02 40512868-42912868
F2:6 qRWCDRI-C02 29.49-31.89 SWUC316 33799496-33799694 3.36 C02 32599496-34999694
F2:6 qRWCDS-C02 29.49-30.89 SWUC316 33799496-33799694 2.77 C02 32599496-34999694
F2:6 qMDADS-C02 29.89-37.57 SWUC316 33799496-33799694 3.35 C02 32599496-34999694
SWUC344 40102848-40103191 2.53 C02 38902848-41303191
SWUC284 43919221-43919418 2.54 C02 42719221-45119418
SWUC293 36909045-36909237
19357230-19357429		 3.00 C02
A02		 35709045-38109237
19177230-19537429
F2:8 qSFWDRI-C03 153.23-157.21 AX-95636893 9150013 2.71 C03 8750013-9550013
F2:6 qSUGDRI-C04 103.69-108.02 AX-95506064 7272757 7.10 C04 6682757-7862757
F2:8 qSUGDS-C06 74.57-101.32 AX-105336545 29172287 3.04 C06 28772287-29572287
AX-95665032 29186383 2.66 C06 28786383-29586383
AX-86230901 29308911 3.04 C06 28908911-29708911
AX-95665273 29401522 3.04 C06 29001522-29801522
AX-95664947 29433854 3.04 C06 29033854-29833854
AX-105310203 29489446 3.04 C06 29089446-29889446
AX-105308711 29627549 3.04 C06 29227549-30027549
AX-86230806 29710301 3.04 C06 29310301-30110301
AX-182145054 29797943 3.04 C06 29397943-30197943
AX-86215830 30202409 3.04 C06 29802409-30602409
AX-86230835 30204371 2.92 C06 29804371-30604371
AX-105308457 30304436 3.04 C06 29904436-30704436
AX-95665820 30314052 3.04 C06 29914052-30714052
AX-105310125 30791904 3.04 C06 30391904-31191904
AX-182087795 31059928 3.04 C06 30659928-31459928
AX-95635741 31183285 3.04 C06 30783285-31583285
AX-86230832 31264725 3.11 C06 30864725-31664725
AX-177912717 31340640 2.95 C06 30940640-31740640
F2:8 qSDWDRI-C09 19.55-37.10 AX-95509234 35782323 2.70 C09 35072323-36492323
AX-86236963 37494562 2.68 C09 36784562-38204562
AX-182158558 46574561 2.68 C09 45864561-47284561

Fig. 5

Analysis of differentially expressed genes of drought-tolerance and drought-sensitivity materials in rapeseed under well water and drought stress A and D: the number of differentially expressed genes and Venn diagram between each time under drought stress and well water in two materials; B and C: the number of differentially expressed genes and Venn diagrams between two materials; E: KEGG enrichment pathway of core differentially expressed genes; F: heatmap of candidate genes related to drought tolerance; No11: drought resistance material; No28: drought sensitivity material; CK: well water; DS24h: 24 h under drought stress; DS36h: 36 h under drought stress; DS48h: 48 h under drought stress."

Fig. 6

Cluster dendrogram and module-trait relationships of WGCNA Abbreviations are the same as those given in Table 1."

Fig. 7

KEGG enrichment pathway in module significant associated with each trait and heatmap of candidate genes related to drought tolerance A: MEdeeppink1; B: MEfirebrick2; C: MEindianred4; D: MEplum; E: heatmap. Abbreviations are the same as those given in Fig. 5."

Table 4

Candidate genes associated with drought tolerance in rapeseed"

QTL 候选基因Candidate gene QTL 候选基因Candidate gene
qSFWCK-A01 BnaA01g08750D (MYC4)
BnaA01g09270D (CHLI1)		 qMDADRI-A09 BnaA09g36380D (RR9)
qRWCDRI-A02 BnaA02g00310D (TGA4) qMDACK-A09 BnaA09g28670D (TEM1)
BnaA09g29410D (PRE6)
qRWCDS-A02 BnaA02g00310D (TGA4) qRWCDS-A09 BnaA09g28670D (TEM1)
BnaA09g29410D (PRE6)
qSFWCK-A02 BnaA02g09540D (RPL24) qRWCCK-A10 BnaA10g01420D (EL22Z)
BnaA10g02050D (PORC)
qSUGCK-A02 BnaA02g27860D (CYP71B22)
BnaA02g27940D (bHLH105)		 qSFWDRI-A10 BnaA10g25310D (SUVH1)
qSDWCK-A02 BnaA02g01690D (RPL10) qSUGCK-C02 BnaC02g20870D (HPA1)
qMDACK-A08 BnaA08g13440D (RPL28C)
BnaA08g14220D (ACO3)		 qMDADS-C02 BnaC02g40790D (KNAT3)
BnaC02g40810D (ERF003)
qSFWDRI-A08 BnaA08g23760D (LHCB6)
BnaA08g25090D (E2-OGDH)
BnaA08g25130D (ADT1)		 qSFWDRI-C03 BnaC03g17470D (PRK1)
BnaC03g17780D (AIP1)
BnaC03g18600D (PXG3)
qSDWCK-A09 BnaA09g04650D (ERF003)
BnaA09g05170D (RUP2)		 qSDWDRI-C09 BnaC09g45770D (RPL37B)
BnaC09g46500D (FLC)
qSFWCK-A09 BnaA09g04650D (ERF003)
BnaA09g05170D (RUP2)
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