植物学报 ›› 2021, Vol. 56 ›› Issue (5): 544-558.DOI: 10.11983/CBB21014
吴丹丹1, 陈永坤1,2, 杨宇1, 孔春艳1, 龚明1,*()
收稿日期:
2021-01-18
接受日期:
2021-05-07
出版日期:
2021-09-01
发布日期:
2021-08-31
通讯作者:
龚明
作者简介:
* E-mail: gongming6307@163.com基金资助:
Dandan Wu1, Yongkun Chen1,2, Yu Yang1, Chunyan Kong1, Ming Gong1,*()
Received:
2021-01-18
Accepted:
2021-05-07
Online:
2021-09-01
Published:
2021-08-31
Contact:
Ming Gong
摘要: 小桐子(Jatropha curcas)是一种极具潜力的能源植物及冷敏植物, 12°C低温锻炼可显著提高其耐冷性。在全基因组水平上对小桐子半胱氨酸蛋白酶家族及靶向其基因的miRNAs进行鉴定、生物信息学分析和表达特性分析, 并对该基因家族成员与miRNAs互作参与调控小桐子对低温锻炼的响应进行解析。结果表明, 在小桐子基因组中共鉴定到39个半胱氨酸蛋白酶基因, 定位于11条染色体上, 可分为6个亚家族(C1A、C2、C12、C13、C14和C15), 编码181-2 158个氨基酸残基的多肽, 均具有Cys和His活性位点。基于miRNA组和降解组测序结果, 发现有283个miRNAs靶向调控小桐子半胱氨酸蛋白酶基因家族的14个成员。对靶向JcDEK1、JcRD21B和JcXBCP3L的miRNAs在12°C低温锻炼过程中的共表达分析表明, 这些miRNAs参与半胱氨酸蛋白酶基因表达的调控, 且这种调控可能与低温锻炼诱导的小桐子耐冷性增强有关。研究结果有助于深入理解小桐子半胱氨酸蛋白酶基因家族功能及其与相应miRNAs的互作, 以及通过互作调控小桐子对低温的响应。
吴丹丹, 陈永坤, 杨宇, 孔春艳, 龚明. 小桐子半胱氨酸蛋白酶家族和相应miRNAs的鉴定及其对低温锻炼的响应. 植物学报, 2021, 56(5): 544-558.
Dandan Wu, Yongkun Chen, Yu Yang, Chunyan Kong, Ming Gong. Identification of the Cysteine Protease Family and Corresponding miRNAs in Jatropha curcas and Their Response to Chill-hardening. Chinese Bulletin of Botany, 2021, 56(5): 544-558.
Primer name | Sequence (5′→ 3′) |
---|---|
miR1314-y-F | GCCGGTCTCCAATGTTAGG |
miR1151-y-F | ATCTGGTTGTGGGACCCG |
miR5156-x-F | GCGAGACTGTGAAACTGCAAA |
miR6483-y-F | GCGTTGTAGAAATTTTCAGGATCA |
JcXBCP3L-F | TCTGTGGGTATGGATGGTTCTGC |
JcXBCP3L-R | ACCCCAGTCAGTACCCCACGA |
JcRD21B-F | CAACGCTTTAGGAGAGAAGGAA |
JcRD21B-R | ACGCAACTTGTTCCTCCTGAC |
JcDEK1-F | TGCTGGGAAATTCTGGTG |
JcDEK1-R | AGCCGTCAAACCCACCA |
Reverse primer | GCTGTCAACGATACGCTACGTAACG |
U6-F | GGAACGATACAGAGAAGATT |
GAPDH-F | TGAAGGACTGGAGAGGTGGAAGAGC |
GAPDH-R | ATCAACAGTTGGAACACGGAAAGCC |
表1 qRT-PCR相关引物
Table 1 The related primers for qRT-PCR
Primer name | Sequence (5′→ 3′) |
---|---|
miR1314-y-F | GCCGGTCTCCAATGTTAGG |
miR1151-y-F | ATCTGGTTGTGGGACCCG |
miR5156-x-F | GCGAGACTGTGAAACTGCAAA |
miR6483-y-F | GCGTTGTAGAAATTTTCAGGATCA |
JcXBCP3L-F | TCTGTGGGTATGGATGGTTCTGC |
JcXBCP3L-R | ACCCCAGTCAGTACCCCACGA |
JcRD21B-F | CAACGCTTTAGGAGAGAAGGAA |
JcRD21B-R | ACGCAACTTGTTCCTCCTGAC |
JcDEK1-F | TGCTGGGAAATTCTGGTG |
JcDEK1-R | AGCCGTCAAACCCACCA |
Reverse primer | GCTGTCAACGATACGCTACGTAACG |
U6-F | GGAACGATACAGAGAAGATT |
GAPDH-F | TGAAGGACTGGAGAGGTGGAAGAGC |
GAPDH-R | ATCAACAGTTGGAACACGGAAAGCC |
Locus ID | Gene name | Subgroup | Chr. | Size (aa) | Mw (Da) | pI |
---|---|---|---|---|---|---|
XM_012209792.1 | JcRD21A | C1A | Chr. 10 | 475 | 52682.16 | 5.39 |
XM_012221410.1 | JcSAG12H4 | C1A | Chr. 4 | 340 | 37417.89 | 5.13 |
XM_012226309.1 | JcSAG12H1 | C1A | Chr. 3 | 311 | 34256.46 | 6.89 |
XM_012216029.1 | JcSAG12H2 | C1A | Chr. 7 | 268 | 28610.75 | 4.66 |
XM_012216557.1 | JcXBCP3 | C1A | Chr. 4 | 441 | 48817.81 | 6.06 |
XM_012218796.1 | JcRD21A1 | C1A | Chr. 10 | 358 | 40417.25 | 5.10 |
XM_012223641.1 | JcALP1 | C1A | Chr. 7 | 347 | 38935.92 | 8.43 |
XM_012225588.1 | JcRD19B | C1A | Chr. 10 | 409 | 44955.43 | 6.71 |
XM_012230158.1 | JcCEP2 | C1A | Chr. 7 | 358 | 39943.84 | 6.19 |
XM_012233098.1 | JcSAG12H5 | C1A | Chr. 9 | 340 | 37592.12 | 5.01 |
XM_012236390.1 | JcXBCP3L | C1A | Chr. 3 | 524 | 58042.85 | 5.24 |
XM_012219020.1 | JcXCP1 | C1A | Chr. 5 | 349 | 39054.13 | 5.59 |
XM_012211812.1 | JcRD19A | C1A | Chr. 2 | 370 | 40564.71 | 5.95 |
XM_012212907.1 | JcRD21B | C1A | Chr. 4 | 466 | 51785.03 | 5.28 |
XM_012213199.1 | JcSAG12H3 | C1A | Chr. 2 | 339 | 37598.38 | 5.94 |
XM_012216569.1 | JcRD19C | C1A | Chr. 4 | 368 | 40923.12 | 5.81 |
XM_012218200.1 | JcXCP2 | C1A | Chr. 4 | 350 | 39176.15 | 5.40 |
XM_012221663.1 | JcTHI1 | C1A | Chr. 11 | 358 | 39435.49 | 5.88 |
XM_012223907.1 | JcRD21C | C1A | Chr. 7 | 366 | 41119.35 | 5.40 |
XM_012224546.1 | JcCEP1 | C1A | Chr. 5 | 360 | 40142.92 | 5.69 |
XM_020685390.1 | JcSAG12H6 | C1A | Chr. 3 | 181 | 20779.04 | 9.49 |
XM_020685389.1 | JcSAG12H7 | C1A | Chr. 3 | 181 | 20779.04 | 9.49 |
XM_012227664.1 | JcCTB1 | C1A | Chr. 8 | 358 | 39709.10 | 6.07 |
XM_012225478.1 | JcDEK1 | C2 | Chr. 1 | 2158 | 239010.06 | 6.03 |
XM_012224060.1 | JcUCH2 | C12 | Chr. 4 | 337 | 38597.28 | 6.43 |
XM_012214672.1 | JcUCH3 | C12 | Chr. 9 | 236 | 26006.51 | 4.66 |
XM_012231737.1 | JcVPE2 | C13 | Chr. 9 | 495 | 55104.34 | 5.58 |
XM_012221936.1 | JcVPE1 | C13 | Chr. 11 | 493 | 54253.23 | 5.93 |
XM_012232060.1 | JcVPE3 | C13 | Chr. 5 | 485 | 54983.84 | 6.22 |
XM_012229170.1 | JcAMC4G | C14 | Chr. 5 | 418 | 45953.22 | 5.18 |
Locus ID | Gene name | Subgroup | Chr. | Size (aa) | Mw (Da) | pI |
XM_012227353.1 | JcAMC9A | C14 | Chr. 3 | 317 | 35221.20 | 5.84 |
XM_012213747.1 | JcAMC3B | C14 | Chr. 2 | 374 | 41063.04 | 5.71 |
XM_012213748.1 | JcAMC1C | C14 | Chr. 2 | 330 | 37646.13 | 8.05 |
XM_012213889.1 | JcAMC2D | C14 | Chr. 2 | 406 | 45165.20 | 8.65 |
XM_012213890.1 | JcAMC1E | C14 | Chr. 2 | 335 | 37746.43 | 8.10 |
XM_012228350.1 | JcAMC1F | C14 | Chr. 8 | 362 | 39681.00 | 6.41 |
XM_012235144.1 | JcAMC1H | C14 | Chr. 5 | 370 | 40503.80 | 6.34 |
XM_012230023.1 | JcPCP1 | C15 | Chr. 7 | 217 | 23577.96 | 6.07 |
XM_012233456.1 | JcPCP2 | C15 | Chr. 6 | 219 | 23969.43 | 6.08 |
表2 小桐子中已鉴定的半胱氨酸蛋白酶的理化性质
Table 2 Physicochemical properties of identified cysteine proteins in Jatropha curcas
Locus ID | Gene name | Subgroup | Chr. | Size (aa) | Mw (Da) | pI |
---|---|---|---|---|---|---|
XM_012209792.1 | JcRD21A | C1A | Chr. 10 | 475 | 52682.16 | 5.39 |
XM_012221410.1 | JcSAG12H4 | C1A | Chr. 4 | 340 | 37417.89 | 5.13 |
XM_012226309.1 | JcSAG12H1 | C1A | Chr. 3 | 311 | 34256.46 | 6.89 |
XM_012216029.1 | JcSAG12H2 | C1A | Chr. 7 | 268 | 28610.75 | 4.66 |
XM_012216557.1 | JcXBCP3 | C1A | Chr. 4 | 441 | 48817.81 | 6.06 |
XM_012218796.1 | JcRD21A1 | C1A | Chr. 10 | 358 | 40417.25 | 5.10 |
XM_012223641.1 | JcALP1 | C1A | Chr. 7 | 347 | 38935.92 | 8.43 |
XM_012225588.1 | JcRD19B | C1A | Chr. 10 | 409 | 44955.43 | 6.71 |
XM_012230158.1 | JcCEP2 | C1A | Chr. 7 | 358 | 39943.84 | 6.19 |
XM_012233098.1 | JcSAG12H5 | C1A | Chr. 9 | 340 | 37592.12 | 5.01 |
XM_012236390.1 | JcXBCP3L | C1A | Chr. 3 | 524 | 58042.85 | 5.24 |
XM_012219020.1 | JcXCP1 | C1A | Chr. 5 | 349 | 39054.13 | 5.59 |
XM_012211812.1 | JcRD19A | C1A | Chr. 2 | 370 | 40564.71 | 5.95 |
XM_012212907.1 | JcRD21B | C1A | Chr. 4 | 466 | 51785.03 | 5.28 |
XM_012213199.1 | JcSAG12H3 | C1A | Chr. 2 | 339 | 37598.38 | 5.94 |
XM_012216569.1 | JcRD19C | C1A | Chr. 4 | 368 | 40923.12 | 5.81 |
XM_012218200.1 | JcXCP2 | C1A | Chr. 4 | 350 | 39176.15 | 5.40 |
XM_012221663.1 | JcTHI1 | C1A | Chr. 11 | 358 | 39435.49 | 5.88 |
XM_012223907.1 | JcRD21C | C1A | Chr. 7 | 366 | 41119.35 | 5.40 |
XM_012224546.1 | JcCEP1 | C1A | Chr. 5 | 360 | 40142.92 | 5.69 |
XM_020685390.1 | JcSAG12H6 | C1A | Chr. 3 | 181 | 20779.04 | 9.49 |
XM_020685389.1 | JcSAG12H7 | C1A | Chr. 3 | 181 | 20779.04 | 9.49 |
XM_012227664.1 | JcCTB1 | C1A | Chr. 8 | 358 | 39709.10 | 6.07 |
XM_012225478.1 | JcDEK1 | C2 | Chr. 1 | 2158 | 239010.06 | 6.03 |
XM_012224060.1 | JcUCH2 | C12 | Chr. 4 | 337 | 38597.28 | 6.43 |
XM_012214672.1 | JcUCH3 | C12 | Chr. 9 | 236 | 26006.51 | 4.66 |
XM_012231737.1 | JcVPE2 | C13 | Chr. 9 | 495 | 55104.34 | 5.58 |
XM_012221936.1 | JcVPE1 | C13 | Chr. 11 | 493 | 54253.23 | 5.93 |
XM_012232060.1 | JcVPE3 | C13 | Chr. 5 | 485 | 54983.84 | 6.22 |
XM_012229170.1 | JcAMC4G | C14 | Chr. 5 | 418 | 45953.22 | 5.18 |
Locus ID | Gene name | Subgroup | Chr. | Size (aa) | Mw (Da) | pI |
XM_012227353.1 | JcAMC9A | C14 | Chr. 3 | 317 | 35221.20 | 5.84 |
XM_012213747.1 | JcAMC3B | C14 | Chr. 2 | 374 | 41063.04 | 5.71 |
XM_012213748.1 | JcAMC1C | C14 | Chr. 2 | 330 | 37646.13 | 8.05 |
XM_012213889.1 | JcAMC2D | C14 | Chr. 2 | 406 | 45165.20 | 8.65 |
XM_012213890.1 | JcAMC1E | C14 | Chr. 2 | 335 | 37746.43 | 8.10 |
XM_012228350.1 | JcAMC1F | C14 | Chr. 8 | 362 | 39681.00 | 6.41 |
XM_012235144.1 | JcAMC1H | C14 | Chr. 5 | 370 | 40503.80 | 6.34 |
XM_012230023.1 | JcPCP1 | C15 | Chr. 7 | 217 | 23577.96 | 6.07 |
XM_012233456.1 | JcPCP2 | C15 | Chr. 6 | 219 | 23969.43 | 6.08 |
图2 小桐子6个半胱氨酸蛋白酶亚家族的蛋白结构 C: 半胱氨酸; D: 天冬氨酸; E: 谷氨酸; H: 组氨酸; N: 天冬酰胺; Q: 谷氨酰胺
Figure 2 Protein structure of the six cysteine protease subfamilies in Jatropha curcas C: Cys; D: Asp; E: Glu; H: His; N: Asn; Q: Gln
图3 使用MEME软件确定的小桐子半胱氨酸蛋白酶家族9个重要的基序 横坐标表示基序的长度; 纵坐标表示基序的保守程度。
Figure 3 The top nine motifs of cysteine protease family in Jatropha curcas identified using the MEME software The abscissa represents the length of the motif; the ordinate indicates the conservatism of the motif.
图4 小桐子半胱氨酸蛋白酶基因染色体定位及成对发生的重复事件 重复基因对用线显示和连接。
Figure 4 Chromosome location and repetitive events of cysteine protease gene pairs in Jatropha curcas Repeated gene pairs are shown and linked by the lines.
图6 小桐子幼苗叶片半胱氨酸蛋白酶家族基因在12°C低温锻炼期间基因表达的热图
Figure 6 Heatmap of gene expression of cysteine protease family in leaves of Jatropha curcas seedlings during chill-hardening at 12°C
图7 miRNAs靶向调控小桐子半胱氨酸蛋白酶家族基因的网络图 红色代表半胱氨酸蛋白酶基因, 蓝色代表miRNAs。
Figure 7 Networks of targeted regulation among miRNAs and their corresponding cysteine protease family genes in Jatropha curcas Red represents cysteine protease gene and blue represents miRNAs.
图8 靶向调控小桐子半胱氨酸蛋白酶家族基因的miRNAs在12°C低温锻炼期间的热图
Figure 8 Heatmap of miRNAs targeting cysteine protease family genes in Jatropha curcas during 12°C chill-hardening
图9 小桐子幼苗在12°C低温锻炼期间半胱氨酸蛋白酶基因JcDEK1、JcRD21B、JcXBCP3L以及靶向这些基因miRNAs的qRT-PCR共表达分析 *与**分别表示不同时间的表达量与对照0小时在P<0.05与P<0.01水平差异显著。
Figure 9 Co-expression analysis by qRT-PCR of the cysteine protease genes JcDEK1, JcRD21B and JcXBCP3L as well as the miRNAs targeting these genes in Jatropha curcas seedlings during chill-hardening at 12°C * and ** indicated the significant differences between the expression level at different time and control 0 h at P<0.05 and P<0.01 level, respectively.
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