Comparative transcriptional profiling analysis of developing melon (Cucumis melo L.) fruit from climacteric and non-climacteric varieties

BMC Genomics

Jordi Garcia-Mas⁵  John Edward Lunn¹  Mark Stitt¹  Yves Gibon²  Christian Larrigaudière³  Manuel Rodriguez-Concepcion⁶  Michael A. Phillips⁶  Joaquin Cañizares⁷  Montserrat Saladié⁴ 

[1] Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Golm, Am Mühlenberg 1, Potsdam 14476, (OT) Golm, Germany;Present address: INRA Bordeaux, University of Bordeaux, UMR1332 Fruit Biology and Pathology, Villenave d’Ornon F-33883, France;IRTA, Parc Científic i Tecnològic Agroalimentari, Parc de Gardeny, Edifici Fruitcentre, Lleida 25003, Spain;Present address: School of Chemistry and Biochemistry, Biochemistry and Molecular Biology, The University of Western Australia, Crawley 6009, WA, Australia;IRTA, Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra, Barcelona 08193, Spain;Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra, Barcelona 08193, Spain;COMAV, Institute for the Conservation and Breeding of Agricultural Biodiversity, Universitat Politècnica de València (UPV), Camino de Vera s/n, Valencia 46022, Spain

关键词: Sucrose;    Microarray;    Fruit development;    Ethylene;    Fruit ripening;    Carotenoids;   

Others  :  1216240
DOI  :  10.1186/s12864-015-1649-3

 received in 2014-10-22, accepted in 2015-05-20,  发布年份 2015

【 摘 要 】

Background

In climacteric fruit-bearing species, the onset of fruit ripening is marked by a transient rise in respiration rate and autocatalytic ethylene production, followed by rapid deterioration in fruit quality. In non-climacteric species, there is no increase in respiration or ethylene production at the beginning or during fruit ripening. Melon is unusual in having climacteric and non-climacteric varieties, providing an interesting model system to compare both ripening types. Transcriptomic analysis of developing melon fruits from Védrantais and Dulce (climacteric) and Piel de sapo and PI 161375 (non-climacteric) varieties was performed to understand the molecular mechanisms that differentiate the two fruit ripening types.

Results

Fruits were harvested at 15, 25, 35 days after pollination and at fruit maturity. Transcript profiling was performed using an oligo-based microarray with 75 K probes. Genes linked to characteristic traits of fruit ripening were differentially expressed between climacteric and non-climacteric types, as well as several transcription factor genes and genes encoding enzymes involved in sucrose catabolism. The expression patterns of some genes in PI 161375 fruits were either intermediate between. Piel de sapo and the climacteric varieties, or more similar to the latter. PI 161375 fruits also accumulated some carotenoids, a characteristic trait of climacteric varieties.

Conclusions

Simultaneous changes in transcript abundance indicate that there is coordinated reprogramming of gene expression during fruit development and at the onset of ripening in both climacteric and non-climacteric fruits. The expression patterns of genes related to ethylene metabolism, carotenoid accumulation, cell wall integrity and transcriptional regulation varied between genotypes and was consistent with the differences in their fruit ripening characteristics. There were differences between climacteric and non-climacteric varieties in the expression of genes related to sugar metabolism suggesting that they may be potential determinants of sucrose content and post-harvest stability of sucrose levels in fruit. Several transcription factor genes were also identified that were differentially expressed in both types, implicating them in regulation of ripening behaviour. The intermediate nature of PI 161375 suggested that classification of melon fruit ripening behaviour into just two distinct types is an over-simplification, and that in reality there is a continuous spectrum of fruit ripening behaviour.

【 授权许可】

   
2015 Saladié et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

Fig. 7.

Fig. 8.

Fig. 9.

【 参考文献 】

• [1]McMurchie EJ, McGlasson WB, Eaks IL. Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature. 1972; 237:235-6.
• [2]Giovannoni JJ. Genetic regulation of fruit development and ripening. Plant Cell. 2004; 16:S170-80.
• [3]Yamaguchi M, Hughes DL, Yabumoto K, Jennings WG. Quality of cantaloupe muskmelons: Variability and attributes. Scientia Hort. 1977; 6:59-70.
• [4]Seymour GB, McGlasson WB. Melons. In: Seymour GB, Taylor JE, Tucker GA, editors. Biochemistry of fruit ripening. London: Chapman & Hall; 1993. p. 273-290.
• [5]Pech JC, Balague C, Latché A, Bouzayen M. Post-harvest physiology of climacteric fruits: recent developments in the biosynthesis and action of ethylene. Sci Aliments. 1994; 14:3-15.
• [6]Latché A, Ayub RA, Martinez G, Guis M, Ben Amor M, Rombaldi CV et al.. Biosynthèse et mode d’action de l’hormone végétale éthylène. Fruits. 1995; 50:379-96.
• [7]Moore S, Payton P, Wright M, Tanksley S, Giovannoni J. Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot. 2005; 56:2885-95.
• [8]Giovannoni JJ. Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol. 2007; 10:283-9.
• [9]Saladié M, Rose JKC, Cosgrove DJ, Catalá C. Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Plant J. 2006; 47:282-95.
• [10]Stepanova AN, Alonso JM. Ethylene signalling and response: where different regulatory modules meet. Curr Opin Plant Sci. 2009; 12:548-55.
• [11]Alexander L, Grierson D. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot. 2002; 53:2039-55.
• [12]Klee HJ. Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol. 2004; 135:660-7.
• [13]Adams-Phillips L, Barry C, Giovannoni J. Signal transduction systems regulating fruit ripening. Trends Plant Sci. 2004; 9:331-8.
• [14]Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R et al.. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science. 2002; 296:343-6.
• [15]Giovannoni JJ, Tanksley S, Vrebalov J, Noensie F. NOR gene compositions and methods for use thereof. US Patent 6762347_B1. July 13, 2004.
• [16]Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ et al.. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet. 2006; 38:948-52.
• [17]Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A. TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J. 2009; 60:1081-95.
• [18]Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D. A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J. 2008; 55:301-10.
• [19]Chung M-Y, Vrebalov J, Alba R, Lee JM, McQuinn R, Chung J-D et al.. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 2011; 64:936-47.
• [20]Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR et al.. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell. 2011; 23:923-41.
• [21]Seymour GB, Chapman NH, Chew BL, Rose JKC. Regulation of ripening and opportunities for control in tomato and other fruits. Plant Biotechnol J. 2013; 11:269-78.
• [22]Klee HJ, Giovannoni JJ. Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet. 2011; 45:41-59.
• [23]Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M et al.. The tomato FRUITFUL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-Independent aspects of fruit ripening. Plant Cell. 2012; 24:4437-51.
• [24]Fujisawa M, Shima Y, Higuchi N, Nakano T, Koyama Y, Kasumi T et al.. Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta. 2012; 235:1107-22.
• [25]Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma A. Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Mol Genet Genom. 2012; 287:189-203.
• [26]Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J et al.. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol. 2013; 31:154-9.
• [27]Wilkinson JQ, Lanahan MB, Conner TW, Klee HJ. Identification of mRNAs with enhanced expression in ripening strawberry fruit using polymerase chain reaction differential display. Plant Mol Biol. 1995; 27:1097-108.
• [28]Manning K. Isolation of a set of ripening-related genes from strawberry: Their identification and possible relationship to fruit quality traits. Planta. 1998; 205:622-31.
• [29]Aharoni A, Keizer LC, Bouwmeester HJ, Sun Z, Alvarez-Huerta M, Verhoeven HA et al.. Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell. 2000; 12:647-62.
• [30]Osorio S, Alba R, Nikoloski Z, Kochevenko A, Fernie AR, Giovannoni JJ. Integrative comparative analyses of transcript and metabolite profiles from pepper and tomato ripening and development stages uncovers species-specific patterns of network regulatory behavior. Plant Physiol. 2012; 159:1713-29.
• [31]Ezura H, Owino WO. Melon ripening and ethylene. Plant Sci. 2008; 175:121-9.
• [32]Pech JC, Bouzayen M, Latché A. Climacteric fruit ripening: ethylene-dependent and independent regulation of ripening pathways in melon fruit. Plant Sci. 2008; 175:114-20.
• [33]Vegas J, Garcia-Mas J, Monforte AJ. Interaction between QTLs induces an advance in ethylene biosynthesis during melon fruit ripening. Theor Appl Genet. 2013; 126:1531-44.
• [34]Lyons JM, Pratt HK, McGlasson WB. Ethylene production, respiration, and internal gas concentrations in cantaloupe fruits at various stages of maturity. Plant Physiol. 1962; 37:31-26.
• [35]Hadfield KA, Dang T, Guis M, Pech JC, Bouzayen M, Bennett AB. Characterization of ripening-regulated cDNAs and their expression in ethylene-suppressed Charentais melon fruit. Plant Physiol. 2000; 122:977-83.
• [36]Ayub R, Guis M, Ben Amor M, Gillot L, Roustan JP, Latché A et al.. Expression of ACC oxidase antisense gene inhibits ripening of cantaloupe melon fruits. Nat Biotechnol. 1996; 14:862-6.
• [37]Monforte AJ, Oliver M, Gonzalo MJ, Alvarez JM, Dolcet-Sanjuan R, Arus P. Identification of quantitative trait loci involved in fruit quality traits in melon (Cucumis melo L.). Theor Appl Genet. 2004; 108:750-8.
• [38]Cuevas HE, Staub JE, Simon PW, Zalapa JE. A consensus linkage map identifies genomic regions controlling fruit maturity and beta-carotene-associated flesh color in melon (Cucumis melo L.). Theor Appl Genet. 2009; 119:741-56.
• [39]Bian W, Barsan C, Egea I, Purgatto E, Chervin C, Zouine M et al.. Metabolic and molecular events occurring during chromoplast biogenesis. J Bot. 2011; 10:1-13.
• [40]Pratt HK, Goeschl JD, Martin FW. Fruit growth and development, ripening, and role of ethylene in honey dew muskmelon. J Am Soc Hortic Sci. 1977; 102:203-10.
• [41]Lester GE, Dunlap JR. Physiological-changes during development and ripening of perlita muskmelon fruits. Sci Hortic. 1985; 26:323-31.
• [42]Rose JKC, Hadfield KA, Labavitch JM, Bennett AB. Temporal sequence of cell wall disassembly in rapidly ripening melon fruit. Plant Physiol. 1998; 117:345-61.
• [43]Nishiyama K, Guis M, Rose JK, Kubo Y, Bennett KA, Wangjin L et al.. Ethylene regulation of fruit softening and cell wall disassembly in Charentais melon. J Exp Bot. 2007; 58:1281-90.
• [44]Portnoy V, Diber A, Pollock S, Karchi H, Lev S, Tzuri G et al.. Use of non-normalized, non-amplified cDNA for 454-based RNA sequencing of fleshy melon fruit. Plant Genome. 2011; 4:1.
• [45]Dai N, Cohen S, Portnoy V, Tzuri G, Harel-Beja R, Pompan-Lotan M et al.. Metabolism of soluble sugars in developing melon fruit: a global transcriptional view of the metabolic transition to sucrose accumulation. Plant Mol Biol. 2011; 76:1-18.
• [46]Corbacho J, Romojaro F, Pech JC, Latché A, Gomez-Jimenez MC. Transcriptomic events involved in melon mature-fruit abscission comprise the sequential induction of cell-wall degrading genes coupled to a stimulation of endo and exocytosis. PLoS One. 2013; 8:e58363.
• [47]Mascarell-Creus A, Cañizares J, Vilarrasa-Blasi J, Mora-García S, Blanca J, Gonzalez-Ibeas D et al.. An oligo-based microarray offers novel transcriptomic approaches for the analysis of pathogen resistance and fruit quality traits in melon (Cucumis melo L). BMC Genomics. 2009; 10:e467. BioMed Central Full Text
• [48]Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, Gonzalez VM et al.. The genome of melon (Cucumis melo L.). Proc Natl Acad Sci U S A. 2012; 109:11872-7.
• [49]Gonzalez-Ibeas D, Cañizares J, Aranda MA. Microarray analysis shows that recessive resistance to Watermelon mosaic virus in melon is associated with the induction of defense response genes. Mol Plant Microbe Interact. 2012; 25:107-18.
• [50]Roig C, Fita A, Ríos G, Hammond JP, Nuez F, Picó B. Root transcriptional responses of two melon genotypes with contrasting resistance to Monosporascus cannonballus (Pollack et Uecker) infection. BMC Genomics. 2012; 13:601-12. BioMed Central Full Text
• [51]Conesa A, Nueda MJ, Ferrer A, Talón M. MaSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics. 2006; 22:1096-102.
• [52]Al-Shahrour F, Díaz-Uriarte R, Dopazo J. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics. 2004; 20:578-80.
• [53]Pilati S, Perazzolli M, Malossini A, Cestaro A, Demattè L, Fontana P et al.. Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at vèraison. BMC Genomics. 2007; 8:428. BioMed Central Full Text
• [54]Miki T, Yamamoto M, Nakagawa H, Ogura N, Mori H, Imaseki H et al.. Nucleotide sequence of a cDNA for 1-aminocyclopropane-1-carboxylate synthase from melon fruits. Plant Physiol. 1995; 107:297-8.
• [55]Yamamoto M, Miki T, Ishiki Y, Fujinami K, Yanagisawa Y, Nakagawa H et al.. The synthesis of ethylene in melon fruit during the early stage of ripening. Plant Cell Physiol. 1995; 36:591-59.
• [56]Lehman A, Black R, Ecker JR. HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell. 1996; 85:183-94.
• [57]Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H. The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. J Exp Bot. 2010; 61(5):1523-35.
• [58]Yang Y, Wu Y, Pirrello J, Regad F, Bouzayen M, Deng W et al.. Silencing Sl-EBF1 and Sl-EBF2 expression causes constitutive ethylene response phenotype, accelerated plant senescence, and fruit ripening in tomato. J Exp Bot. 2010; 61(3):697-708.
• [59]Tanaka R, Oster U, Kruse E, Rudiger W, Grimm B. Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase. Plant Physiol. 1999; 120:695-704.
• [60]Kim J, DellaPenna D. Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid beta-ring hydroxylase CYP97A3. Proc Natl Acad Sci U S A. 2006; 103:3474-9.
• [61]Welsch R, Maass D, Voegel T, Dellapenna D, Beyer P. Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol. 2007; 145:1073-85.
• [62]Neta-Sharir I, Isaacson T, Lurie S, Weiss D. Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell. 2005; 17:1829-38.
• [63]Li L, Paolillo DJ, Parthasarathy MV, Dimuzio EM, Garvin DF. A novel gene mutation that confers abnormal patterns of beta-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J. 2001; 26:59-67.
• [64]Lu S, Van Eck J, Zhou X, Lopez AB, Halloran DM, Cosman KM et al.. The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of beta-carotene accumulation. Plant Cell. 2006; 18:3594-605.
• [65]Akhtar MS, Goldschmidt EE, John I, Rodoni S, Matile P, Grierson D. Altered patterns of senescence and ripening in gf, a stay-green mutant of tomato. J Exp Bot. 1999; 50(336):1115-22.
• [66]Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N et al.. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003; 34:374-8.
• [67]Lohse M, Nunes-Nesi A, Krüger P, Nagel A, Hannemann J, Giorgi FM et al.. Robin: an intuitive wizard application for R-based expression microarray quality assessment and analysis. Plant Physiol. 2010; 153:642-51.
• [68]Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P et al.. MapMan: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004; 37:914-39.
• [69]Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M. A guide to using MapMan to visualize and compare omics data in plants: a case study in the crop species, maize. Plant Cell Environ. 2009; 32:1211-29.
• [70]Costa F, Alba R, Schouten H, Soglio V, Gianfranceschi L, Serra S et al.. Use of homologous and heterologous gene expression profiling tools to characterize transcription dynamics during apple fruit maturation and ripening. BMC Plant Biol. 2010; 10:229. BioMed Central Full Text
• [71]Zhang C, Yu X, Ayre BG, Turgeon R. The origin and composition of cucurbit “phloem” exudate. Plant Physiol. 2012; 158:1873-82.
• [72]Rose JKC, Saladié M, Catalá C. The plot thickens: new perspectives of primary cell wall modification. Current Opin Plant Biol. 2004; 7:296-301.
• [73]Manning K. Changes in gene-expression during strawberry fruit ripening and their regulation by auxin. Planta. 1994; 194:62-8.
• [74]Saladié M, Wright LP, Garcia-Mas J, Rodriguez-Concepcion M, Phillips MA. The 2-C-methylerithritol 4-phosphate pathway in melon is regulated by specialized isoforms for the first and last steps. J Exp Bot. 2014; 65:5077-92.
• [75]Périn C, Gomez-Jimenez M, Hagen L, Dogimont C, Pech JC, Latché A et al.. Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit. Plant Physiol. 2002; 129:300-9.
• [76]Eduardo I, Arús P, Monforte AJ. Development of a genomic library of near isogenic lines (NILs) in melon (Cucumis melo L.) from the exotic accession PI161375. Theor Appl Genet. 2005; 112:139-48.
• [77]Stitt M, McLilley R, Gerhardt R, Heldt HW. Metabolite levels in specific cells and subcellular compartments of plant leaves. Meth Enzymol. 1989; 174:518-52.
• [78]Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A et al.. Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry. 2006; 67:1579-89.
• [79]Rodriguez-Concepcion M, Fores O, Martinez-Garcia JF, Gonzalez V, Phillips MA, Ferrer A et al.. Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell. 2004; 16:144-56.
• [80]Fraser PD, Pinto MES, Holloway DE, Bramley PM. Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J. 2000; 24:551-8.
• [81]Burns J, Fraser PD, Bramley PM. Identification and quantification of carotenoids, tocopherols and chlorophylls in commonly consumed fruits and vegetables. Phytochemistry. 2003; 62:939-47.
• [82]Taylor KL, Brackenridge AE, Vivier MA, Oberholster A. High-performance liquid chromatography profiling of the major carotenoids in Arabidopsis thaliana leaf tissue. J Chromatogr A. 2006; 1121:83-91.
• [83]Hartigan JA, Wong MA. A k-means clustering algorithm. Appl Stat. 1979; 28:100-8.
• [84]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al.. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25:25-9.
• [85]Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A et al.. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002; 3:0034.1. BioMed Central Full Text
• [86]Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations. Biotechnol Lett. 2004; 26:509-15.
• [87]Gonzalez-Ibeas D, Blanca J, Roig C, González-To M, Picó B, Truniger V et al.. MELOGEN: An EST database for melon functional genomics. BMC Genomics. 2007; 8:306. BioMed Central Full Text
• [88]Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29:e45.
• [89]Masoudi-Nejad A, Goto S, Jauregui R, Ito M, Kawashima S, Moriya Y et al.. EGENES: transcriptome-based plant database of genes with metabolic pathway information and expressed sequence tag indices in KEGG. Plant Physiol. 2007; 144:857-66.
• [90]Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N et al.. Extension of the visualisation tool MapMan to allow statistical analysis of arrays, display of corresponding genes and comparison with known responses. Plant Physiol. 2005; 138:1195-204.
• [91]Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol. 1995; 57:289-300.