Mapping and transcriptomic profiling reveal that the KNAT6 gene is involved in the dark green peel colour of mature pumpkin fruit (Cucurbita maxima L.).
Journal
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik
ISSN: 1432-2242
Titre abrégé: Theor Appl Genet
Pays: Germany
ID NLM: 0145600
Informations de publication
Date de publication:
17 Sep 2024
17 Sep 2024
Historique:
received:
04
07
2024
accepted:
06
09
2024
medline:
18
9
2024
pubmed:
17
9
2024
entrez:
17
9
2024
Statut:
epublish
Résumé
We identified a 580 bp deletion of CmaKNAT6 coding region influences peel colour of mature Cucurbita maxima fruit. Peel colour is an important agronomic characteristic affecting commodity quality in Cucurbit plants. Genetic mapping of fruit peel colour promotes molecular breeding and provides an important basis for understanding the regulatory mechanism in Cucurbit plants. In the present study, the Cucurbita maxima inbred line '9-6' which has a grey peel colour and 'U3-3-44' which has a dark green peel colour in the mature fruit stage, were used as plant materials. At 5-40 days after pollination (DAP), the contents of chlorophyll a, chlorophyll b, total chlorophyll and carotenoids in the 'U3-3-44' peels were significantly greater than those in the '9-6' peels. In the epicarp of the '9-6' mature fruit, the presence of nonpigmented cell layers and few chloroplasts in each cell in the pigmented layers were observed. Six generations derived by crossing '9-6' and 'U3-3-44' were constructed, and the dark green peel was found to be controlled by a single dominant locus, which was named CmaMg (mature green peel). Through bulked-segregant analysis sequencing (BSA-seq) and insertion-deletion (InDel) markers, CmaMg was mapped to a region of approximately 449.51 kb on chromosome 11 using 177 F
Identifiants
pubmed: 39287784
doi: 10.1007/s00122-024-04741-7
pii: 10.1007/s00122-024-04741-7
doi:
Substances chimiques
Plant Proteins
0
Chlorophyll
1406-65-1
Carotenoids
36-88-4
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
225Subventions
Organisme : National Natural Science Foundation of China
ID : 32072590
Organisme : National Natural Science Foundation of China
ID : 32272723
Organisme : National Natural Science Foundation of China
ID : 31872124
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106
pubmed: 20979621
pmcid: 3218662
Ballester AR, Molthoff J, de Vos R et al (2009) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol 152:71–84
pubmed: 19906891
Barros L, Dueñas M, Pinela J et al (2012) Characterization and quantification of Phenolic compounds in four tomato (Lycopersicon esculentum L.) farmers’ varieties in Northeastern portugal homegardens. Plant Foods Hum Nutr 67:229–234
pubmed: 22922837
Barry CS, McQuinn RP, Chung MY et al (2008) Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol 147:179–187
pubmed: 18359841
pmcid: 2330295
Belles-Boix E, Hamant O, Witiak SM, Morin H, Traas J, Pautot V (2006) KNAT6: an Arabidopsis homeobox gene involved in meristem activity and organ separation. Plant Cell 18:1900–1907
pubmed: 16798887
pmcid: 1533965
Chayut N, Yuan H, Ohali S, Meir A, Sa’ar U, Tzuri G, Zheng Y, Mazourek M, Gepstein S, Zhou X, Portnoy V, Lewinsohn E, Schaffer AA, Katzir N, Fei Z, Welsch R, Li L, Burger J, Tadmor Y (2017) Distinct mechanisms of the ORANGE protein in controlling carotenoid flux. Plant Physiol 173:376–389
pubmed: 27837090
Chomicki G, Schaefer H, Renner SS (2020) Origin and domestication of Cucurbitaceae crops: insights from phylogenies, genomics and archaeology. New Phytol 226:1240–1255
pubmed: 31230355
Cortleven A, Schmülling T (2015) Regulation of chloroplast development and function by cytokinin. J Exp Bot 66:4999–5013
pubmed: 25873684
DeLuca DS, Levin JZ, Sivachenko A, Fennell T, Nazaire M-D, Williams C, Reich M, Winckler W, Getz G (2012) RNA-SeQC: RNA-seq metrics for quality control and process optimization. Bioinformatics 28:1530–1532
pubmed: 22539670
pmcid: 3356847
Ding W, Wang Y, Qi C, Luo Y, Wang C, Xu W, Qu S (2021) Fine mapping identified the gibberellin 2-oxidase gene CpDw leading to a dwarf phenotype in squash (Cucurbita pepo L.). Plant Sci 306:110857
pubmed: 33775356
Ding W, Luo Y, Li W, Chen F, Wang C, Xu W, Wang Y, Qu S (2024) Fine mapping and transcriptome profiling reveal CpAPRR2 to modulate immature fruit rind color formation in zucchini (Cucurbita pepo). Theor Appl Genet 137(7):167
pubmed: 38909110
Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14:547–558
pubmed: 11910003
pmcid: 150578
Duan Y, Xiang C, Liu X, Ma W, Sun T, Wang C (2017) Effect of rind structure and pigment composition on rind color in Cucurbita maxima (in Chinese). China Veg 11:33–39
Ezin V, Gbemenou UH, Ahanchede A (2022) Characterization of cultivated pumpkin (Cucurbita moschata Duchesne) landraces for genotypic variance, heritability and agromorphological traits. Saudi J Biol Sci 29:3661–3674
pubmed: 35844434
pmcid: 9280217
Feder A, Burger J, Gao S, Lewinsohn E, Katzir N, Schaffer AA, Meir A, Davidovich-Rikanati R, Portnoy V, Gal-On A, Fei Z, Kashi Y, Tadmor Y (2015) A kelch domain-containing F-box coding gene negatively regulates flavonoid accumulation in muskmelon. Plant Physiol 169:1714–1726
pubmed: 26358418
pmcid: 4634078
Fekih R, Takagi H, Tamiru M, Abe A, Natsume S, Yaegashi H, Sharma S, Sharma S, Kanzaki H, Matsumura H, Saitoh H, Mitsuoka C, Utsushi H, Uemura A, Kanzaki E, Kosugi S, Yoshida K, Cano L, Kamoun S, Terauchi R (2013) MutMap+: genetic mapping and mutant identification without crossing in rice. PLoS ONE 8:1–10
Fernandez-Moreno JP, Tzfadia O, Forment J et al (2016) Characterization of a new pink-fruited tomato mutant results in the identification of a null allele of the SlMYB12 transcription factor. Plant Physiol 171:1821–1836
pubmed: 27208285
pmcid: 4936558
Ge Y, Li X, Yang XX, Cui CS, Qu SP (2015) Short communication genetic linkage map of Cucurbita maxima with molecular and morphological markers. Genet Mol Res 14:5480–5484
pubmed: 26125744
Hao N, Du Y, Li H, Wang C, Wang C, Gong S, Zhou S, Wu T (2018) CsMYB36 is involved in the formation of yellow green peel in cucumber (Cucumis sativus L.). Theor Appl Genet 131:1659–1669
pubmed: 29740668
Hay A, Tsiantis M (2010) KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–3165
pubmed: 20823061
Hill JT, Demarest BL, Bisgrove BW (2013) MMAPPR: mutation mapping analysis pipeline for pooled RNA-seq. Genome Res 23:687–697
pubmed: 23299975
pmcid: 3613585
Hwang I, Kim Y, Han J, Nou IS (2016) Orange color is associated with CYC-B expression in tomato fleshy fruit. Mol Breeding 36:42
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485
pubmed: 16664080
pmcid: 1064541
Jeong H-B, Jang S-J, Kang MY et al (2020) Candidate gene analysis reveals that the fruit color locus C1 corresponds to PRR2 in pepper (Capsicum frutescens). Front Plant 11:399
Kang SI, Rahim MA, Afrin KS et al (2018) Expression of anthocyanin biosynthesis-related genes reflects the peel color in purple tomato. Hortic Environ Biotechnol 59:435–445
Kiramana JK, Isutsa DK (2017) First detailed morphological characterisation of qualitative traits of extensive naturalized pumpkin germplasm in Kenya. Int J Dev Sci 6:500–525
Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y et al (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749
pubmed: 17337630
pmcid: 1867377
Li J, Li G, Gao S, Martinez C, He G, Zhou Z et al (2010) Arabidopsis transcription factor ELONGATED HYPOCOTYL5 plays a role in the feedback regulation of phytochrome A signaling. Plant Cell 22:3634–3649
pubmed: 21097709
pmcid: 3015127
Li Y, Wen C, Weng Y (2013) Fine mapping of the pleiotropic locus B for black spine and orange mature fruit color in cucumber identifies a 50 kb region containing a R2R3-MYB transcription factor. Theor Appl Genet 126:2187–2196
pubmed: 23689749
Li B, Zhao S, Dou J, Ali A, Gebremeskel H, Gao L, He N, Lu X, Liu W (2019) Genetic mapping and development of molecular markers for a candidate gene locus controlling rind color in watermelon. Theor Appl Genet 132:2741–2753
pubmed: 31286160
Liu H, Meng H, Pan Y, Liang X, Jiao J, Li Y, Chen S, Cheng Z (2015) Fine genetic mapping of the white immature fruit color gene w to a 33.0-kb region in cucumber (Cucumis sativus L.). Theor Appl Genet 128:2375–2385
pubmed: 26239410
Liu H, Jiao J, Liang X, Liu J, Meng H, Chen S, Li Y, Cheng Z (2016) Map-based cloning, identification and characterization of the w gene controlling white immature fruit color in cucumber (Cucumis sativus L.). Theor Appl Genet 129:1247–1256
pubmed: 26934889
Liu D, Yang H, Yuan Y, Zhu H, Zhang M, Wei X, Sun D, Wang X, Yang S, Yang L (2020) Comparative transcriptome analysis provides insights into yellow rind formation and preliminary mapping of the Clyr (yellow rind) gene in watermelon. Front Plant Sci 11:192
pubmed: 32218790
pmcid: 7078170
Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69
pubmed: 8538741
Lun Y, Wang X, Zhang C, Yang L, Gao D, Chen H, Huang S (2016) A CsYcf54 variant conferring light green coloration in cucumber. Euphytica 208:509–517
Luo F, Cheng S-C, Cai J-H et al (2019) Chlorophyll degradation and carotenoid biosynthetic pathways: gene expression and pigment content in broccoli during yellowing. Food Chem 297:124964
pubmed: 31253313
Lux A, Morita S, Abe J, Ito K (2005) An improved method for clearing and staining free-hand sections and whole-mount samples. Ann Bot 96:989–996
pubmed: 16192293
pmcid: 4247103
Ma L, Liu Z, Cheng Z, Gou J, Chen J, Yu W, Wang P (2021) Identification and application of BhAPRR2 controlling peel colour in wax gourd (Benincasa hispida). Front Plant Sci 12:716772
pubmed: 34659288
pmcid: 8517133
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
pubmed: 20644199
pmcid: 2928508
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628
pubmed: 18516045
Nadakuduti SS, Holdsworth WL, Klein CL, Barry CS (2014) KNOX genes influence a gradient of fruit chloroplast development through regulation of GOLDEN2-LIKE expression in tomato. Plant J 78:1022–1033
pubmed: 24689783
Nguyen CV, Vrebalov JT, Gapper NE et al (2014) Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening. Plant Cell 26:585–601
pubmed: 24510723
pmcid: 3967027
Niu J, Chen Q, Lu X, Wang X, Tang Z, Liu Q, Lei F, Xu X (2023) Fine mapping and identifying candidate gene of Y underlying yellow peel in Cucurbita pepo. Front Plant Sci 14:1159937
pubmed: 37152148
pmcid: 10160447
Oren E, Tzuri G, Vexler L, Dafna A, Meir A, Faigenboim A, Kenigswald M, Portnoy V, Schaffer AA, Levi A, Buckler ES, Katzir N, Burger J, Tadmor Y, Gur A (2019) The multi-allelic APRR2 gene is associated with fruit pigment accumulation in melon and watermelon. J Exp Bot 70:3781–3794
pubmed: 31175368
pmcid: 6685648
Ouyang X, Li J, Li G, Li B, Chen B, Shen H et al (2011) Genome-wide binding site analysis of FAR-RED ELONGATED HYPOCOTYL3 reveals its novel function in Arabidopsis development. Plant Cell 23:2514–2535
pubmed: 21803941
pmcid: 3226222
Parnis A, Cohen O, Gutfinger T, Hareven D, Zamir D, Lifschitz E (1997) The dominant developmental mutants of tomato, Mouse-ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 9:2143–2158
pubmed: 9437860
pmcid: 157064
Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11:1650–1667
pubmed: 27560171
pmcid: 5032908
Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15:8–15
Ragni L, Belles-Boix E, Günl M, Pautot V (2008) Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis inflorescences. Plant Cell 20:888–900
pubmed: 18390591
pmcid: 2390738
Ruckle ME, DeMarco SM, Larkin RM (2007) Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19:3944–3960
pubmed: 18065688
pmcid: 2217644
Salamov AA, Solovyev VV (2000) Ab initio gene finding in drosophila genomic DNA. Genome Res 10(4):516
pubmed: 10779491
pmcid: 310882
Scofield S, Dewitte W, Murray JA (2007) The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis. Plant J 50:767–781
pubmed: 17461793
Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V, Proveniers M, Aalen RB, Butenko MA (2011) Arabidopsis class I KNOTTED-like homeobox proteins act downstream in the IDA-HAE/HSL2 floral abscission signaling pathway. Plant Cell 23:2553–2567
pubmed: 21742991
pmcid: 3226213
Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019–2025
pubmed: 17487191
Sun X, Wang B, Gu S, Wang Z (2003) Correlations of immature skin color and pigments in cucumber. Hortic Plant J 6:721
Sun X, Xie F, Chen Y, Guo Z, Dong L, Qin L, Shi Z, Xiong L, Yuan R, Deng W, Jiang Y (2022) Glutamine synthetase gene PpGS1.1 negatively regulates the powdery mildew resistance in Kentucky bluegrass. Hortic Res 9:196
Tadmor Y, Burger J, Yaakov I, Feder A, Libhaber SE, Portnoy V, Meir A, Tzuri G, Sa’ar U, Rogachev I, Aharoni A, Abeliovich H, Schaffer AA, Lewinsohn E, Katzir N (2010) Genetics of flavonoid, carotenoid, and chlorophyll pigments in melon fruit rinds. J Agric Food Chem 58:10722–10728
pubmed: 20815398
Tanaka R, Kobayashi K, Masuda T (2011) Tetrapyrrole Metabolism in Arabidopsis thaliana. Arabidopsis Book 9:145
Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, Martienssen R, Selvaraj G, Datla R (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci U S A 99:4730–4735
pubmed: 11917137
pmcid: 123716
Wang H, Wang H (2015) Multifaceted roles of FHY3 and FAR1 in light signaling and beyond. Trends Plant Sci 20:453–461
pubmed: 25956482
Wang C, Li W, Chen F, Cheng Y, Huang X, Zou B, Wang Y, Xu W, Qu S (2022) Genome-wide identification and characterization of members of the ACS gene family in Cucurbita maxima and their transcriptional responses to the specific treatments. Int J Mol Sci 23:8476
pubmed: 35955610
pmcid: 9369044
Xanthopoulou A, Montero-Pau J, Mellidou I, Kissoudis C, Blanca J, Picó B, Tsaballa A, Tsaliki E, Dalakouras A, Paris HS, Ganopoulou M, Moysiadis T, Osathanunkul M, Tsaftaris A, Madesis P, Kalivas A, Ganopoulos I (2019) Whole-genome resequencing of Cucurbita pepo morphotypes to discover genomic variants associated with morphology and horticulturally valuable traits. Hortic Res 6:94
pubmed: 31645952
pmcid: 6804688
Yoo H, Park W, Lee G-M et al (2017) Inferring the genetic determinants of fruit colors in tomato by carotenoid profiling. Molecules 22:764
pubmed: 28481314
pmcid: 6154295
Zhao G, Lian Q, Zhang Z, Fu Q, He Y, Ma S, Ruggieri V, Monforte AJ, Wang P, Julca I, Wang H, Liu J, Xu Y, Wang R, Ji J, Xu Z, Kong W, Zhong Y, Shang J, Pereira L, Argyris J, Zhang J, Mayobre C, Pujol M, Oren E, Ou D, Wang J, Sun D, Zhao S, Zhu Y, Li N, Katzir N, Gur A, Dogimont C, Schaefer H, Fan W, Bendahmane A, Fei Z, Pitrat M, Gabaldón T, Lin T, Garcia-Mas J, Xu Y, Huang S (2019) A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat Genet 51:1607–1615
pubmed: 31676864
Zheng Y, Wu S, Bai Y, Sun H, Jiao C, Guo S, Zhao K, Blanca J, Zhang Z, Huang S, Xu Y, Weng Y, Mazourek M, Reddy UK, Ando K, McCreight JD, Schaffer AA, Burger J, Tadmor Y, Katzir N, Tang X, Liu Y, Giovannoni JJ, Ling KS, Wechter WP, Levi A, Garcia-Mas J, Grumet R, Fei Z (2019) Cucurbit Genomics Database (CuGenDB): a central portal for comparative and functional genomics of cucurbit crops. Nucleic Acids Res 47(D1):D1128–D1136
pubmed: 30321383
Zhong YJ, Zhou YY, Li JX, Yu T, Wu TQ, Luo JN, Luo SB, Huang HX (2017) A high-density linkage map and QTL mapping of fruit-related traits in pumpkin (Cucurbita moschata Duch.). Sci Rep 7:12785
pubmed: 28986571
pmcid: 5630576
Zhu L, Wang Y, Zhang Z, Hu D, Wang Z, Hu J, Ma C, Yang L, Sun S, Li Y (2022) Chromosomal fragment deletion in APRR2-repeated locus modulates the dark stem color in Cucurbita pepo. Theor Appl Genet 135:4277–4288
pubmed: 36098750