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Non-climacteric fruit ripening in pepper: increased transcription of EIL-like genes normally regulated by ethylene

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Abstract

Only limited information has been published to date on the similarities and differences between climacteric and non-climacteric fruit ripening on transcriptional level. To address this issue, we performed a direct comparative transcriptome analysis between tomato and pepper fruits using heterologous microarray hybridization. Given the significant differences in the morphological, physiological, and biochemical characteristics of pepper and tomato fruits, the existence of extensive common regulons is surprising. This finding suggests the conservation of ripening mechanisms in climacteric and non-climacteric fruits. However, disparate expression profiles were also observed in both fruits. This study revealed that a gene that encodes an enzyme that converts lycopene to downstream carotenoids is induced in pepper but not in tomato. Most of the genes that encode ribosomal proteins are only induced in early fruit-stage pepper fruit and show rapidly diminishing expression in the later developmental stages. The genes involved in ethylene biosynthesis were not induced in pepper fruit. However, the EIL-like genes, ethylene-mediated signaling components, were induced in pepper fruit. Divergent types of transcription factors were expressed in ripening tomato and pepper fruits, suggesting they may be key factors that differentiate these distinct ripening processes.

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References

  • Aharoni A, O’Connell AP (2002) Gene expression analysis of strawberry achene and receptacle maturation using DNA microarray. J Exp Bot 53:2073–2087

    Article  PubMed  CAS  Google Scholar 

  • Aharoni A, Keizer LC, Van Den Broeck HC, Blanco-Portales R, Munoz-Blanco J, Bois G, Smit P, De Vos RC, O’Connell AP (2002) Novel insight into vascular, stress, and auxin-dependent and -independent gene expression programs in strawberry, a non-climacteric fruit. Plant Physiol 129:1019–1031

    Article  PubMed  CAS  Google Scholar 

  • Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin G, Tanksley S, Giovannoni J (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control tomato fruit development. Plant Cell 17:2954–2965

    Article  PubMed  CAS  Google Scholar 

  • Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055

    Article  PubMed  CAS  Google Scholar 

  • Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268

    PubMed  CAS  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340

    Article  PubMed  CAS  Google Scholar 

  • Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15:2165–2180

    Article  PubMed  CAS  Google Scholar 

  • Carrington CMS, Greve LC, Labavitch JM (1993) Cell wall metabolism in ripening fruit. VI. Effect of the antisense polygalacturonase gene on cell wall changes accompanying ripening in transgenic tomatoes. Plant Physiol 103:429–434

    PubMed  CAS  Google Scholar 

  • Carrari F, Fernie AR, Iusem ND (2004) Heard it through the grapevine? ABA and sugar cross-talk: the ASR story. Trends Plant Sci 9:57–59

    Article  PubMed  CAS  Google Scholar 

  • Chen G, Alexander L, Grierson D (2004) Constitutive expression of EIL-like transcription factor partially restores ripening in the ethylene-institutive Nr tomato mutant. J Exp Bot 402:1491–1497

    Article  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U S A 81:1991–1995

    Article  PubMed  CAS  Google Scholar 

  • Clendennen SK, May GD (1997) Differential gene expression in ripening banana fruit. Plant Physiol 115:463–469

    Article  PubMed  CAS  Google Scholar 

  • Davies C, Boss PK, Robinson SP (1997) Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115:1155–1161

    PubMed  CAS  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • El Kereamy A, Chervin C, Roustan JP, Cheynier V, Souquet JM, Moutounet M, Raynal J, Ford C, Latché A, Pech JC, Bouzayen M (2003) Exogenous ethylene stimulates the long-term expression of genes related to anthocyanin biosynthesis in grape berries. Physiol Plant 119:175–182

    Article  CAS  Google Scholar 

  • Fei Z, Tang X, Alba RM, White JA, Ronning CM, Martin GB, Tanksley SD, Giovannoni J (2004) Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J 40:47–59

    Article  PubMed  Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80

    Article  PubMed  Google Scholar 

  • Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mo Biol 52:725–749

    Article  CAS  Google Scholar 

  • Giovannoni J (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(Suppl):S170–S180

    Article  PubMed  CAS  Google Scholar 

  • Girke T, Todd J, Ruuska S, White J, Benning C, Ohlrogge J (2000) Microarray analysis of developing Arabidopsis seeds. Plant Physiol 124:1570–1581

    Article  PubMed  CAS  Google Scholar 

  • Gu J, Gu X (2003) Induced gene expression in human brain after the split from chimpanzee. Trends Genet 19:63–65

    Article  PubMed  CAS  Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    Article  PubMed  CAS  Google Scholar 

  • Horn R, Lecouls AC, Callahan A, Dandekar A, Garay L, McCord P, Howad W, Chan H, Verde I, Main D, Jung S, Georgi L, Forrest S, Mook J, Zhebentyayeva T, Yu Y, Kim HR, Jesudurai C, Sosinski B, Arus P, Baird V, Parfitt D, Reighard G, Scorza R, Tomkins J, Wing R, Abbott AG (2005) Candidate gene database and transcript map for peach, a model species for fruit trees. Theor Appl Genet 110:1419–1428

    Article  PubMed  Google Scholar 

  • Hornero-Mendez D, Minguez-Mosquera MI (2000) Xanthophyll esterification accompanying carotenoid overaccumulation in chromoplast of Capsicum annuum ripening fruits is a constitutive process and useful for ripeness index. J Agric Food Chem 48:1617–1622

    Article  PubMed  CAS  Google Scholar 

  • Jaakola L, Maatta K, Pirttila AM, Torronen R, Karenlampi S, Hohtola A (2002) Expression of genes involved in anthocyanin biosynthesis in relation to anthocyanin, proanthocyanidin, and flavonol levels during bilberry fruit development. Plant Physiol 130:729–739

    Article  PubMed  CAS  Google Scholar 

  • Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002) Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214:751–758

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Ishmaru M, Hirapka K, Honda C (2002) Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215:924–933

    Article  PubMed  CAS  Google Scholar 

  • Lawrence SD, Cline K, Moore GA (1997) Chromoplast development in ripening tomato fruit: identification of cDNAs for chromoplast-targeted proteins and characterization of a cDNA encoding a plastid-localized low-molecular-weight heat shock protein. Plant Mol Biol 33:483–492

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Kim SY, Chung E, Joung YH, Pai HS, Hur CG, Choi D (2004) EST and microarray analyses of pathogen responsive genes in pepper (Capsicum annuum L.) non-host resistance against in soybean pustule pathogen (Xanthomonas axonopodis pv. glycines). Funct Integr Genomics 4:196–205

    Article  PubMed  Google Scholar 

  • Leek JT, Monsen E, Dabney AR, Storey JD (2006) EDGE: extraction and analysis of differential gene expression. Bioinformatics 22:507–508

    Article  PubMed  CAS  Google Scholar 

  • Livingstone KD, Lackney VK, Blauth JR, van Wijk R, Jahn MK (1999) Genome mapping in capsicum and the evolution of genome structure in the Solanaceae. Genetics 152:1183–1202

    PubMed  CAS  Google Scholar 

  • Manning K (1998) Isolation of a set of ripening-related genes from strawberry: their identification and possible relationship to fruit quality traits. Planta 205:622–631

    Article  PubMed  CAS  Google Scholar 

  • Mao L, Begum D, Chuang HW, Budiman MA, Szymkowiak EJ, Irish EE, Wing RA (2000) JOINTLESS is a MADS-box gene in tomato controlling flower abscission zone development. Nature 406:910–913

    Article  PubMed  CAS  Google Scholar 

  • Marin-Rodriguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53:2115–2119

    Article  PubMed  CAS  Google Scholar 

  • Moody DE, Zou Z, McIntyre L (2002) Cross-species hybridization of pig RNA to human nylon microarrays. BMC Genomics 3:27

    Article  PubMed  CAS  Google Scholar 

  • Moore S, Vrebalov J, Payton P, Giovannoni J (2002) Use of genomics tools to isolate key ripening genes and analyses fruit maturation in tomato. J Exp Bot 53:2023–2030

    Article  PubMed  CAS  Google Scholar 

  • Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarray for comparative gene expression analysis in the Solanaceae. J Exp Bot 56:2885–2895

    Article  PubMed  CAS  Google Scholar 

  • Moyle RL, Crowe ML, Ripi-Koia J, Fairbairn DJ, Botella JR (2005a) PineappleDB: an online pineapple bioinformatics resource. BMC Plant Biol 5:21

    Article  PubMed  CAS  Google Scholar 

  • Moyle RL, Fairbairn DJ, Ripi J, Crowe M, Botella JR (2005b) Developing pineapple fruit has a small transcriptome dominated by metallothionein. J Exp Bot 56:101–112

    PubMed  CAS  Google Scholar 

  • Nairn CJ, Niedz RP, Hearn CJ, Osswald WF, Mayer RT (1997) cDNA cloning and expression of a class II acidic chitinase from sweet orange. Biochim Biophys Acta 1351:22–26

    PubMed  CAS  Google Scholar 

  • Nam YW, Tichit L, Leperlier M, Cuerq B, Marty I, Lelievre JM (1999) Isolation and characterization of mRNAs differentially expressed during ripening of wild strawberry (Fragaria vesca L.) fruits. Plant Mol Biol 39:629–636

    Article  PubMed  CAS  Google Scholar 

  • Nowrousian M, Ringelberg C, Dunlap JC, Loros JJ, Kück U (2005) Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospore. Mol Genet Genomics 273:137–149

    Article  PubMed  CAS  Google Scholar 

  • Oh BJ, Kim KD, Kim YS (1998) A microscopic characterization of the infection of green and red pepper fruits by an isolate of Colletotrichum gloeosporioides. J Phytopathol 146:301–303

    Article  Google Scholar 

  • Perin C, Gomez-Jimenez M, Hagen L, Dogimont C, Pech JC, Latche A, Pitrat M, Lelievre JM (2002) Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit. Plant Physiol 129:300–309

    Article  PubMed  CAS  Google Scholar 

  • Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL (2003) Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300:1742–1745

    Article  PubMed  CAS  Google Scholar 

  • Rasori A, Ruperti B, Bonghi C, Tonutti P, Ramina A (2002) Characterization of two putative ethylene receptor genes expressed during peach fruit development and abscission. J Exp Bot 53:2333–2339

    Article  PubMed  CAS  Google Scholar 

  • Ray J, Knapp J, Grierson D, Bird C, Schuch W (1988) Identification and sequence determination of a cDNA clone for tomato pectinesterase. Eur J Biochem 174:119–124

    Article  PubMed  CAS  Google Scholar 

  • Rhodes MJC (1988) The maturation and ripening of fruits. In: Thiman KV (ed) Senescence in plant. CRC Press, Bocca Raton, pp 157–205

    Google Scholar 

  • Rise ML, von Schalburg KR, Brown GD, Mawer MA et al (2004) Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Genome Res 14:478–490

    Article  PubMed  Google Scholar 

  • Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378

    PubMed  CAS  Google Scholar 

  • Saltveit ME (1977) Carbon dioxide, ethylene and color development in ripening mature green bell peppers. J Am Soc Hortic Sci 102:523–525

    CAS  Google Scholar 

  • Salzman RA, Tikhonova I, Bordelon BP, Hasegawa PM, Bressan RA (1998) Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape. Plant Physiol 117:465–472

    Article  PubMed  CAS  Google Scholar 

  • Schmidt R (2002) Plant genome evolution: lesion from comparative genomics at the DNA level. Plant Mol Biol 48:21–37

    Article  PubMed  CAS  Google Scholar 

  • Seymour GB, Taylor JE, Tucker GA (1993) Biochemistry of fruit ripening. Chapman and Hall, London

    Google Scholar 

  • Sitrit Y, Bennett AB (1998) Regulation of tomato fruit galacturonase mRNA accumulation by ethylene: a re-examination. Plant Physiol 116:1145–1150

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, Bernatzky R, Lapitan NL, Prince JP (1988) Conservation of gene repertoire but not gene order in pepper and tomato. Proc Natl Acad Sci U S A 85:6419–6423

    Article  PubMed  CAS  Google Scholar 

  • Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Leon C, Renaudin JP, Dedaldechamp F, Romieu C, Delrot S, Hamdi S (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222:832–847

    Article  PubMed  CAS  Google Scholar 

  • Tesniere C, Pradal M, El-Kereamy A, Torregrosa L, Chatelet P, Roustan JP, Chervin C (2004) Involvement of ethylene signaling in a non-climacteric fruit: new elements regarding the regulation of ADH expression in grapevine. J Exp Bot 55:2235–2240

    Article  PubMed  CAS  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98:5116–5121

    Article  PubMed  CAS  Google Scholar 

  • Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, de Vos CH, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106

    Article  PubMed  CAS  Google Scholar 

  • Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343–346

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Dooley TP, Curto EV, Davis RL, VandeBerg JL (2004) Cross-species application of cDNA microarrays to profile gene expression using UV-induced melanoma in Monodelphis domestica as the model system. Genomics 83:588–599

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latche A, Pech JC, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692

    Article  PubMed  CAS  Google Scholar 

  • Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Hoffman N (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol Plant Mol Biol 35:155–189

    Article  CAS  Google Scholar 

  • Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latch A, Pech JC, Bouzayen M (1999) Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display. Plant J 18:589–600

    Article  PubMed  CAS  Google Scholar 

  • Zhong J, Barbour AG (2003) Cross-species hybridization of a Borrelia burgdorferi DNA array reveals infection- and culture-associated genes of the unsequenced genome of the relapsing fever agent Borrelia hermsii. Mol Microbiol 51:729–748

    Article  CAS  Google Scholar 

  • Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that binds a cis-element of pathogenesis-related genes. EMBO J 16:3207–3218

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to Drs. Woo-Taek Kim, Hwa-Jee Chung, Youn Lee, and Jim Giovannoni for helpful discussion and for critical reading of the manuscript. This work was supported by grants from PDRC (PF0033-01) and CFGC (CG1431) of the 21st Century Frontier Research Program, funded by MOST of the Korean government.

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Correspondence to Doil Choi.

Electronic supplementary materials

All of the array data used in this study was deposited in ArrayExpress under the accession number E-MEXP-260.

Figure S1

A figure showing a quality control analysis of replicated microarray experiments. (GIF 456 kb)

High resolution image (TIFF 985 kb)

Table S1

A complete list of fruit-specific genes in pepper and tomato. (XLS 352 kb)

Table S2

Genes encoding ribosomal proteins that are up- or down-regulated more than twofold during fruit ripening. (XLS 41 kb)

Table S3

Genes that are differently regulated in the early fruit stages of pepper and tomato. (XLS 106 kb)

Table S4

Genes that are differently regulated in the mature green fruit stages of pepper and tomato. (XLS 90 kb)

Table S5

Genes that are differently regulated in the breaker fruit stages of pepper and tomato. (XLS 112 kb)

Table S6

Genes that are differently regulated in the red ripe fruit stages of pepper and tomato. (XLS 80 kb)

Table S7

Genes used in the comparative expression analysis of pepper and tomato ripening. (XLS 822 kb)

Table S8

Genes used in the comparative expression analysis that showed up- or down-regulation of over twofold during pepper or tomato ripening. (XLS 345 kb)

Table S9

A table of pair-wise correlation coefficients of the replicated array data. (DOC 133 kb)

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Lee, S., Chung, EJ., Joung, YH. et al. Non-climacteric fruit ripening in pepper: increased transcription of EIL-like genes normally regulated by ethylene. Funct Integr Genomics 10, 135–146 (2010). https://doi.org/10.1007/s10142-009-0136-9

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