植物学报 ›› 2025, Vol. 60 ›› Issue (4): 515-532.DOI: 10.11983/CBB24112 cstr: 32102.14.CBB24112
赵蔓雅, 孙倩楠, 徐晶晶, 段恬妮, 蔡锦涛, 周婧, 范婷婷, 萧浪涛*(), 王若仲*(
)
收稿日期:
2024-07-23
接受日期:
2025-06-04
出版日期:
2025-07-10
发布日期:
2025-06-04
通讯作者:
萧浪涛,王若仲
基金资助:
Manya Zhao, Qiannan Sun, Jingjing Xu, Tianni Duan, Jintao Cai, Jing Zhou, Tingting Fan, Langtao Xiao*(), Ruozhong Wang*(
)
Received:
2024-07-23
Accepted:
2025-06-04
Online:
2025-07-10
Published:
2025-06-04
Contact:
Langtao Xiao, Ruozhong Wang
摘要: 叶色突变体是研究光形态发生、叶绿体发育、叶绿素代谢和光合作用机制等多种生理过程的理想材料。该研究从黄瓜(Cucumis sativus) XYYH-2-1-1株系自交后代中获得1个新的黄化致死突变体ycl (yellow cotyledon lethal)。该突变体自幼苗出土后子叶一直呈黄化状态, 约2周后枯萎死亡, 其生长抑制表型为非光依赖型。与野生型相比, ycl突变体的Chl a和Chl b含量趋于零, 叶绿素生物合成途径中Mg2+螯合过程受阻。显微和超微结构分析发现, ycl叶片组织紊乱、叶绿体发育受阻。ycl的抗氧化酶活性及丙二醛含量显著升高, 说明其受到氧化胁迫, 且抗氧化能力强。ycl净光合速率极显著降低, 胞间CO2浓度上升, 推测ycl光合速率降低源于气孔导度降低、叶绿素含量减少和叶绿体发育受阻。转录组学分析表明, ycl与其野生型间存在337个差异表达基因, 光合作用、类黄酮生物合成、叶绿素代谢和活性氧代谢是导致ycl黄化致死表型形成的关键途径。通过BSA-Seq分析, ycl突变基因初步定位于3号染色体的1.48-1.9 Mb区间, 内含41个候选基因。对ycl突变体的研究为阐明黄瓜叶绿体发育的分子机制提供了参考。
赵蔓雅, 孙倩楠, 徐晶晶, 段恬妮, 蔡锦涛, 周婧, 范婷婷, 萧浪涛, 王若仲. 一个新的黄瓜叶色突变体鉴定、初定位及转录组分析. 植物学报, 2025, 60(4): 515-532.
Manya Zhao, Qiannan Sun, Jingjing Xu, Tianni Duan, Jintao Cai, Jing Zhou, Tingting Fan, Langtao Xiao, Ruozhong Wang. Identification, Mapping and Transcriptome Analysis of a New Leaf Color Mutant in Cucumber. Chinese Bulletin of Botany, 2025, 60(4): 515-532.
Primer name | Forward primer (5′→3′) | Reverse primer (5'→3') |
---|---|---|
Cs-Actin | GTTACGCCCTCCCTCATGCCATTC | TCCCGTTCGGCAGTGGTGGT |
CsaV3_3G002180 | GTCGTCCTGCCATTCGATCA | AGCACCAAGTTCACTCCAACT |
CsaV3_5G025230 | AATTCTTCCGACCCGAACCC | AGTAGCCTTCTGCGGACCTA |
CsaV3_1G030370 | CAGTGGCTGGATACGTCCTC | GTGAGCTCCCGCCATAAAGT |
CsaV3_7G000620 | TGGAGCATCTCCGAAAGTGG | GGCAAGGAATTGTGATGCCA |
CsaV3_5G028880 | TAGAACCCAGGCTCCCTCAA | CCGTGTTTTCACAAGCTTCTCT |
CsaV3_3G041340 | AACATGTTACTGGTGGGGGC | CACATTGAAATCATTGGGTACCTG |
CsaV3_6G037230 | CCCACTCAAGCGATGTG CTA | CCATTGACCTCAGCATTGCG |
CsaV3_5G006200 | GACCCAGTTCAAGCTAGCCA | ACTGAGACAACAAGCGCGTA |
CsaV3_7G008610 | GGCTCCAAGGGCCAATACAT | GTAGGCCTTGGACAGGCATT |
表1 qRT-PCR引物
Table 1 Primers used for qRT-PCR
Primer name | Forward primer (5′→3′) | Reverse primer (5'→3') |
---|---|---|
Cs-Actin | GTTACGCCCTCCCTCATGCCATTC | TCCCGTTCGGCAGTGGTGGT |
CsaV3_3G002180 | GTCGTCCTGCCATTCGATCA | AGCACCAAGTTCACTCCAACT |
CsaV3_5G025230 | AATTCTTCCGACCCGAACCC | AGTAGCCTTCTGCGGACCTA |
CsaV3_1G030370 | CAGTGGCTGGATACGTCCTC | GTGAGCTCCCGCCATAAAGT |
CsaV3_7G000620 | TGGAGCATCTCCGAAAGTGG | GGCAAGGAATTGTGATGCCA |
CsaV3_5G028880 | TAGAACCCAGGCTCCCTCAA | CCGTGTTTTCACAAGCTTCTCT |
CsaV3_3G041340 | AACATGTTACTGGTGGGGGC | CACATTGAAATCATTGGGTACCTG |
CsaV3_6G037230 | CCCACTCAAGCGATGTG CTA | CCATTGACCTCAGCATTGCG |
CsaV3_5G006200 | GACCCAGTTCAAGCTAGCCA | ACTGAGACAACAAGCGCGTA |
CsaV3_7G008610 | GGCTCCAAGGGCCAATACAT | GTAGGCCTTGGACAGGCATT |
图1 ycl与XYYH-3-1黄瓜子叶期表型变化比较 (A) 4、5、6、7、8和14天野生型(WT)和ycl表型变化(自然光); (B) 第7天苗龄时2组WT和ycl表型差异(黑暗处理7天); (C) 第8天苗龄时2组WT和ycl表型差异(光照培养1天)。Bars=1 cm
Figure 1 Comparison of phenotypic changes between ycl and XYYH-3-1 at the cotyledon stage of cucumber (A) Phenotypic changes of wild type (WT) and ycl in 4, 5, 6, 7, 8 and 14 days (natural light); (B) Phenotypic differences of WT and ycl between the two groups at 7 d of age (dark treatment for 7 d); (C) Phenotypic differences of WT and ycl between the two groups at 8 d of age (light culture for 1 d). Bars=1 cm
Material | Plant height (cm) | Root length (cm) | Stem diameter (cm) | Leaf area (cm2) |
---|---|---|---|---|
WT | 4.86±0.32 | 15.56±0.94 | 0.22±0.03 | 9.04±1.66 |
ycl | 2.64±0.56** | 5.5±0.9** | 0.18±0.02* | 1.95±0.26** |
表2 ycl与XYYH-3-1黄瓜子叶期(7天)的农艺性状
Table 2 Agronomic characters of ycl and XYYH-3-1 at cotyledon stage (7 d) of cucumber
Material | Plant height (cm) | Root length (cm) | Stem diameter (cm) | Leaf area (cm2) |
---|---|---|---|---|
WT | 4.86±0.32 | 15.56±0.94 | 0.22±0.03 | 9.04±1.66 |
ycl | 2.64±0.56** | 5.5±0.9** | 0.18±0.02* | 1.95±0.26** |
图2 ycl与XYYH-3-1叶绿素及其合成中间代谢产物的含量 (A) 叶绿素合成中间代谢产物的相对含量; (B)光合色素含量。WT: 野生型; 5-ALA: 5-氨基乙酰丙酸; PBG: 胆色素原; Urogen III: 尿卟啉原III; Coprogen III: 粪卟啉原III; Proto IX: 原卟啉IX; Mg-Proto IX: Mg-原卟啉IX。*表示差异显著(t检验, P<0.05); **表示差异极显著(t检验, P<0.01); ns表示差异不显著。
Figure 2 Content of chlorophyll and its biosynthetic intermediate metabolites in ycl and XYYH-3-1 (A) Relative content of chlorophyll biosynthetic intermediate metabolites; (B) Photosynthetic pigment content. WT: Wild type; 5-ALA: 5-aminolevulinic acid; PBG: Porphobilinogen; Urogen III: Uroporphyrinogen III; Coprogen III: Coproporphyrinogen III; Proto IX: Protoporphyrin IX; Mg-Proto IX: Mg-protoporphyrin IX. * denote significant differences (t-test, P<0.05); ** denote extremely significant differences (t-test, P<0.01); ns denote no significant difference.
Material | Chl a (mg·g−1) | Chl b (mg·g−1) | Caro (mg·g−1) | Total Chl (mg·g−1) | Chl a/b | Total Chl/Caro |
---|---|---|---|---|---|---|
WT | 0.6483±0.0162 | 0.2157±0.0063 | 0.1304±0.0018 | 0.8641±0.0225 | 3.0057 | 6.6272 |
ycl | 0.0008±0** | 0.0004±0** | 0.0265±0.0007** | 0.0012±0** | 1.9303 | 0.0443 |
表3 ycl和XYYH-3-1叶片的光合色素含量
Table 3 Photosynthetic pigment content in leaves of ycl and XYYH-3-1
Material | Chl a (mg·g−1) | Chl b (mg·g−1) | Caro (mg·g−1) | Total Chl (mg·g−1) | Chl a/b | Total Chl/Caro |
---|---|---|---|---|---|---|
WT | 0.6483±0.0162 | 0.2157±0.0063 | 0.1304±0.0018 | 0.8641±0.0225 | 3.0057 | 6.6272 |
ycl | 0.0008±0** | 0.0004±0** | 0.0265±0.0007** | 0.0012±0** | 1.9303 | 0.0443 |
图3 ycl和XYYH-3-1叶片的显微结构及叶绿体超微结构 (A), (B) 野生型子叶显微结构; (C), (D) 突变体子叶显微结构; (E), (F) 野生型叶绿体超微结构; (G), (H) ycl叶绿体超微结构。(F)是(E)中红色圆圈中的叶绿体放大版。(H)是(G)中红色圆圈中的叶绿体放大版。Sg: 淀粉粒; TH: 类囊体; GL: 基粒片层; O: 嗜锇体
Figure 3 Microstructure and chloroplast ultrastructure of ycl and XYYH-3-1 leaves (A), (B) Wild type cotyledon microstructures; (C), (D) Mutant cotyledon microstructures; (E), (F) Wild type chloroplast ultrastructures; (G), (H) ycl chloroplast ultrastructures. (F) is an enlarged version of the chloroplast in the red circle in (E). (H) is an enlarged version of the chloroplast in the red circle in (G). Sg: Starch grain; TH: Thylakoid; GL: Grana lamella; O: Osmiophilic body
Material | Pn (μmol·m-2·s-1) | Gs (mmol·m-2·s-1) | Ci (μmol·mol-1) | Tr (mol·m-2·s-1) |
---|---|---|---|---|
WT | 15.85±1.39 | 0.37±0.08 | 331±12 | 4.53±0.62 |
ycl | -2.49±0.15** | 0.14±0.02** | 458±7** | 2.17±0.31** |
表4 ycl和XYYH-3-1植株的光合作用参数
Table 4 Photosynthesis parameters of the ycl and XYYH-3-1
Material | Pn (μmol·m-2·s-1) | Gs (mmol·m-2·s-1) | Ci (μmol·mol-1) | Tr (mol·m-2·s-1) |
---|---|---|---|---|
WT | 15.85±1.39 | 0.37±0.08 | 331±12 | 4.53±0.62 |
ycl | -2.49±0.15** | 0.14±0.02** | 458±7** | 2.17±0.31** |
图4 ycl和XYYH-3-1植株的抗氧化物酶活性及丙二醛含量 (A) 超氧化物歧化酶(SOD)活性; (B) 过氧化物酶(POD)活性; (C) 丙二醛(MDA)含量。WT: 野生型. **表示差异极显著(t检验, P<0.01)。
Figure 4 Antioxidant enzyme activities and malondialdehyde contents of ycl and XYYH-3-1 (A) Superoxide dismutase (SOD) activity; (B) Peroxidase (POD) activity; (C) Malondialdehyde (MDA) contents. WT: Wild type. ** denote extremely significant differences (t-test, P<0.01).
图5 突变基因的初定位及筛选 (A)-(C) 单核苷酸多态性分布((A) 第18号群体; (B) XY子叶群体; (C) XY真叶群体); (D) CsaV3_3G001980相对表达量(**表示差异极显著, t检验, P<0.01); (E)-(G) SNP index峰图((E) 第18号群体; (F) XY子叶群体; (G) XY真叶群体)。WT: 野生型; SNP: 单核苷酸多态性
Figure 5 Preliminary localisation and screening of mutant genes (A)-(C) Distribution of single nucleotide polymorphisms ((A) Population 18; (B) XY cotyledon population; (C) XY true leaf population); (D) Relative expression of CsaV3_3G001980 (** denote extremely significant differences, t-test, P<0.01); (E)-(G) SNP index plot ((E) Population 18; (F) XY cotyledon population; (G) XY true leaf population). WT: Wild type; SNP: Single nucleotide polymorphism
Genes within the interval | Annotation |
---|---|
CsaV3_3G001960 | Cytochrome P450 family ent-kaurenoic acid oxidase |
CsaV3_3G001970 | Cytochrome P450 family ent-kaurenoic acid oxidase |
CsaV3_3G001980 | Protein NRT1/PTR FAMILY 7.3-like |
CsaV3_3G001990 | Hsp90 co-chaperone Cdc37, N-terminally processed like |
CsaV3_3G002000 | Ribose-phosphate pyrophosphokinase |
CsaV3_3G002010 | Type I inositol polyphosphate 5-phosphatase, puta |
CsaV3_3G002020 | Phenylalanine-tRNA ligase alpha subunit like |
CsaV3_3G002030 | Two-component response regulator-like aprr2 |
CsaV3_3G002040 | S-adenosyl-L-methionine-dependent methyltransferases superfamily protein |
CsaV3_3G002050 | Vacuolar protein sorting-associated protein 55 homolog |
CsaV3_3G002060 | Haloacid dehalogenase-like hydrolase |
CsaV3_3G002070 | Haloacid dehalogenase-like hydrolase domain-containing protein |
CsaV3_3G002080 | Regulator of nonsense transcripts 1 homolog |
CsaV3_3G002090 | Lon protease homolog 2, peroxisomal |
CsaV3_3G002100 | Electron carrier/iron ion-binding protein |
CsaV3_3G002110 | BOI-related E3 ubiquitin-protein ligase 1 |
CsaV3_3G002120 | Protein of unknown function (DUF581) |
CsaV3_3G002130 | Poly(U)-specific endoribonuclease |
CsaV3_3G002140 | Methyltransferase-like protein 13 |
CsaV3_3G002150 | Beta-amylase |
CsaV3_3G002160 | Protein kinase, putative |
CsaV3_3G002170 | Novel plant snare, putative |
CsaV3_3G002180 | Phosphatidylinositol 4-phosphate 5-kinase 1 |
CsaV3_3G002190 | Coiled-coil domain-containing protein 97 |
CsaV3_3G002200 | Calcineurin B-like protein |
CsaV3_3G002210 | Unknown protein |
CsaV3_3G002220 | Protein kinase |
CsaV3_3G002230 | Unknown protein |
CsaV3_3G002240 | Bifunctional inhibitor/plant lipid transfer protein/seed storage helical domain-containing protein |
CsaV3_3G002250 | Peptidyl-prolyl cis-trans isomerase-like |
CsaV3_3G002260 | DVA-1 polyprotein |
CsaV3_3G002270 | tRNA/rRNA methyltransferase (SpoU) family protein |
CsaV3_3G002280 | Protein lingerer like |
CsaV3_3G002290 | Chlorophyll a/b binding family protein |
CsaV3_3G002300 | ATP-dependent Clp protease proteolytic subunit |
CsaV3_3G002310 | Unknown protein |
CsaV3_3G002320 | Histone-lysine N-methyltransferase, H3 lysine-9 specific SUVH6-like |
CsaV3_3G002330 | Kelch repeat-containing protein |
CsaV3_3G002340 | GATA transcription factor 26-like |
CsaV3_3G002350 | Vesicle-associated protein 2-1 |
CsaV3_3G002360 | 50S ribosomal protein L19, chloroplastic |
表5
ycl突变位点初定位区间内基因 Figure 5 The genes within the preliminarily mapped region of ycl mutant site
Genes within the interval | Annotation |
---|---|
CsaV3_3G001960 | Cytochrome P450 family ent-kaurenoic acid oxidase |
CsaV3_3G001970 | Cytochrome P450 family ent-kaurenoic acid oxidase |
CsaV3_3G001980 | Protein NRT1/PTR FAMILY 7.3-like |
CsaV3_3G001990 | Hsp90 co-chaperone Cdc37, N-terminally processed like |
CsaV3_3G002000 | Ribose-phosphate pyrophosphokinase |
CsaV3_3G002010 | Type I inositol polyphosphate 5-phosphatase, puta |
CsaV3_3G002020 | Phenylalanine-tRNA ligase alpha subunit like |
CsaV3_3G002030 | Two-component response regulator-like aprr2 |
CsaV3_3G002040 | S-adenosyl-L-methionine-dependent methyltransferases superfamily protein |
CsaV3_3G002050 | Vacuolar protein sorting-associated protein 55 homolog |
CsaV3_3G002060 | Haloacid dehalogenase-like hydrolase |
CsaV3_3G002070 | Haloacid dehalogenase-like hydrolase domain-containing protein |
CsaV3_3G002080 | Regulator of nonsense transcripts 1 homolog |
CsaV3_3G002090 | Lon protease homolog 2, peroxisomal |
CsaV3_3G002100 | Electron carrier/iron ion-binding protein |
CsaV3_3G002110 | BOI-related E3 ubiquitin-protein ligase 1 |
CsaV3_3G002120 | Protein of unknown function (DUF581) |
CsaV3_3G002130 | Poly(U)-specific endoribonuclease |
CsaV3_3G002140 | Methyltransferase-like protein 13 |
CsaV3_3G002150 | Beta-amylase |
CsaV3_3G002160 | Protein kinase, putative |
CsaV3_3G002170 | Novel plant snare, putative |
CsaV3_3G002180 | Phosphatidylinositol 4-phosphate 5-kinase 1 |
CsaV3_3G002190 | Coiled-coil domain-containing protein 97 |
CsaV3_3G002200 | Calcineurin B-like protein |
CsaV3_3G002210 | Unknown protein |
CsaV3_3G002220 | Protein kinase |
CsaV3_3G002230 | Unknown protein |
CsaV3_3G002240 | Bifunctional inhibitor/plant lipid transfer protein/seed storage helical domain-containing protein |
CsaV3_3G002250 | Peptidyl-prolyl cis-trans isomerase-like |
CsaV3_3G002260 | DVA-1 polyprotein |
CsaV3_3G002270 | tRNA/rRNA methyltransferase (SpoU) family protein |
CsaV3_3G002280 | Protein lingerer like |
CsaV3_3G002290 | Chlorophyll a/b binding family protein |
CsaV3_3G002300 | ATP-dependent Clp protease proteolytic subunit |
CsaV3_3G002310 | Unknown protein |
CsaV3_3G002320 | Histone-lysine N-methyltransferase, H3 lysine-9 specific SUVH6-like |
CsaV3_3G002330 | Kelch repeat-containing protein |
CsaV3_3G002340 | GATA transcription factor 26-like |
CsaV3_3G002350 | Vesicle-associated protein 2-1 |
CsaV3_3G002360 | 50S ribosomal protein L19, chloroplastic |
图6 ycl与XYYH-3-1间的RNA-Seq分析 (A) 差异表达基因火山图; (B) 差异表达基因KEGG途径富集散点图; (C) GO term二级分类统计结果; (D) 转录组结果的qRT-PCR验证。BP: 生物过程; MF: 分子功能; CC: 细胞组分; WT: 野生型; DEG: 差异表达基因; FPKM: 每千碱基转录本每百万映射片段数; FC: 倍性变化。**表示差异极显著(t检验, P<0.01)。
Figure 6 RNA-Seq analysis of differential expression between ycl and XYYH-3-1 (A) Differentially expressed genes volcano map; (B) Scatter plot of differentially expressed genes KEGG pathway enrichment; (C) GO term secondary classification statistics; (D) The qRT-PCR verification of transcriptome results. BP: Biological process; MF: Molecular function; CC: Cellular component; WT: Wild type; DEG: Differential expressed gene; FPKM: Fragments per kilobase per million mapped reads; FC: Fold Change. ** denote extremely significant differences (t-test, P<0.01).
图7 与ycl表型相关的差异表达基因(DEGs) (A) 涉及光合作用的DEGs; (B) 涉及类黄酮生物合成的DEGs; (C) 涉及花青素转运的DEGs; (D) 编码转录因子的DEGs。WT: 野生型; LHCP: 叶绿素a/b结合蛋白; PC: 质体蓝素; PEPC: 磷酸烯醇式丙酮酸羧化酶; Chlase1: 叶绿素酶1; SAT: 司替木丹碱-O-乙酰转移酶; CCoAMT: 咖啡酰辅酶A-3-O甲基转移酶; GST: 谷胱甘肽S-转移酶; MATE: 多药和有毒物排出家族
Figure 7 Differentially expressed genes (DEGs) associated with the ycl phenotype (A) DEGs involved in photosynthesis; (B) DEGs involved in flavonoid biosynthesis; (C) DEGs involved in anthocyanin transport; (D) DEGs encoding transcription factors. WT: Wild type; LHCP: Chlorophyll a/b binding protein; PC: Plastocyanin; PEPC: Phosphoenolpyruvate carboxylase; Chlase1: Chlorophyllase 1; SAT: Stemmadenine O-acetyltransferase; CCoAMT: Trans- caffeoyl-CoA 3-O-methyltransferase; GST: Glutathione-S-transferase; MATE: Multidrug and toxic compound extrusion
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