Integrative Comparative Analyses of Transcript and Metabolite Profiles from Pepper and Tomato Ripening and Development Stages Uncovers Species-Specific Patterns of Network Regulatory Behavior[W][OA]

Integrative comparative analyses of transcript and metabolite levels from climacteric and nonclimacteric fruits can be employed to unravel the similarities and differences of the underlying regulatory processes. To this end, we conducted combined gas chromatography-mass spectrometry and heterologous microarray hybridization assays in tomato (Solanum lycopersicum; climacteric) and pepper (Capsicum chilense; nonclimacteric) fruits across development and ripening. Computational methods from multivariate and network-based analyses successfully revealed the difference between the covariance structures of the integrated data sets. Moreover, our results suggest that both fruits have similar ethylene-mediated signaling components; however, their regulation is different and may reflect altered ethylene sensitivity or regulators other than ethylene in pepper. Genes involved in ethylene biosynthesis were not induced in pepper fruits. Nevertheless, genes downstream of ethylene perception such as cell wall metabolism genes, carotenoid biosynthesis genes, and the never-ripe receptor were clearly induced in pepper as in tomato fruit. While signaling sensitivity or actual signals may differ between climacteric and nonclimacteric fruit, the evidence described here suggests that activation of a common set of ripening genes influences metabolic traits. Also, a coordinate regulation of transcripts and the accumulation of key organic acids, including malate, citrate, dehydroascorbate, and threonate, in pepper fruit were observed. Therefore, the integrated analysis allows us to uncover additional information for the comprehensive understanding of biological events relevant to metabolic regulation during climacteric and nonclimacteric fruit development.

[1]  D. Choi,et al.  Non-climacteric fruit ripening in pepper: increased transcription of EIL-like genes normally regulated by ethylene , 2010, Functional & Integrative Genomics.

[2]  Yves Gibon,et al.  GMD@CSB.DB: the Golm Metabolome Database , 2005, Bioinform..

[3]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[4]  Joachim Selbig,et al.  Extension of the Visualization Tool MapMan to Allow Statistical Analysis of Arrays, Display of Coresponding Genes, and Comparison with Known Responses1 , 2005, Plant Physiology.

[5]  L. Howard 9 Antioxidant Vitamin and Phytochemical Content of Fresh and Processed Pepper Fruit (Capsicum annuum) , 2007 .

[6]  V. Germain,et al.  Changes in Transcriptional Profiles Are Associated with Early Fruit Tissue Specialization in Tomato1[w] , 2005, Plant Physiology.

[7]  J. Giovannoni,et al.  MOLECULAR BIOLOGY OF FRUIT MATURATION AND RIPENING. , 2001, Annual review of plant physiology and plant molecular biology.

[8]  A. Fernie,et al.  Profiling primary metabolites of tomato fruit with gas chromatography/mass spectrometry. , 2012, Methods in molecular biology.

[9]  Donald J. Nevins,et al.  Changes in physical properties and cell wall polysaccharides of tomato (Lycopersicon esculentum) pericarp tissues , 1993 .

[10]  R. Gómez-Ladrón de Guevara,et al.  Carotenoid biosynthesis changes in five red pepper (Capsicum annuum L.) cultivars during ripening. Cultivar selection for breeding. , 2000, Journal of agricultural and food chemistry.

[11]  N. Hoffman,et al.  Ethylene biosynthesis and its regulation in higher plants , 1984 .

[12]  D. Goodenowe,et al.  Nontargeted metabolome analysis by use of Fourier Transform Ion Cyclotron Mass Spectrometry. , 2002, Omics : a journal of integrative biology.

[13]  E. Olmos,et al.  Characterisation and changes in the antioxidant system of chloroplasts and chromoplasts isolated from green and mature pepper fruits. , 2009, Plant biology.

[14]  J. Labavitch,et al.  Temporal sequence of cell wall disassembly in rapidly ripening melon fruit , 1998, Plant physiology.

[15]  F. Carrari,et al.  Metabolic regulation underlying tomato fruit development. , 2006, Journal of experimental botany.

[16]  Sang-Ho Chung,et al.  Overaccumulation of higher polyamines in ripening transgenic tomato fruit revives metabolic memory, upregulates anabolism-related genes, and positively impacts nutritional quality. , 2007, Journal of AOAC International.

[17]  A. Fernie,et al.  Reconfiguration of the Achene and Receptacle Metabolic Networks during Strawberry Fruit Development1[C][W] , 2008, Plant Physiology.

[18]  J. Rose,et al.  The plot thickens: New perspectives of primary cell wall modification. , 2004, Current opinion in plant biology.

[19]  D. Brummell Cell wall disassembly in ripening fruit. , 2006, Functional plant biology : FPB.

[20]  Mark Stitt,et al.  A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. , 2009, Plant, cell & environment.

[21]  M. Saniewski,et al.  The effect of methyl jasmonate on ethylene production and CO2 evolution in Jonagold apples , 2013 .

[22]  Tadashi Eguchi,et al.  Metabolite profiling of plant carotenoids using the matrix-assisted laser desorption ionization time-of-flight mass spectrometry. , 2007, The Plant journal : for cell and molecular biology.

[23]  A. Mattoo,et al.  Maturity and ripening-stage specific modulation of tomato (Solanum lycopersicum) fruit transcriptome , 2010, GM crops.

[24]  Jerome Grimplet,et al.  Tissue-specific mRNA expression profiling in grape berry tissues , 2007, BMC Genomics.

[25]  W. Vriezen,et al.  Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. , 2007, The New phytologist.

[26]  W. Krzanowski Between-Groups Comparison of Principal Components , 1979 .

[27]  R. Suau,et al.  Partial demethylation of oligogalacturonides by pectin methyl esterase 1 is required for eliciting defence responses in wild strawberry (Fragaria vesca). , 2007, The Plant journal : for cell and molecular biology.

[28]  Paxton Payton,et al.  Use of genomics tools to isolate key ripening genes and analyse fruit maturation in tomato. , 2002, Journal of experimental botany.

[29]  S. Kondo,et al.  Changes of endogenous jasmonic acid and methyl jasmonate in apples and sweet cherries during fruit development. , 2000 .

[30]  S. Blankenship,et al.  Ethylene and Carbon Dioxide Production in Detached Fruit of Selected Pepper Cultivars , 1999 .

[31]  M. Zanor,et al.  RNA Interference of LIN5 in Tomato Confirms Its Role in Controlling Brix Content, Uncovers the Influence of Sugars on the Levels of Fruit Hormones, and Demonstrates the Importance of Sucrose Cleavage for Normal Fruit Development and Fertility1[W][OA] , 2009, Plant Physiology.

[32]  A. Bennett,et al.  Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. , 1999, Trends in plant science.

[33]  D. M. Beckles,et al.  ADP-glucose pyrophosphorylase is located in the plastid in developing tomato fruit. , 2001, Plant physiology.

[34]  D. Hornero-Méndez,et al.  Xanthophyll esterification accompanying carotenoid overaccumulation in chromoplast of Capsicum annuum ripening fruits is a constitutive process and useful for ripeness index. , 2000, Journal of agricultural and food chemistry.

[35]  A. Bombarely,et al.  Generation and analysis of ESTs from strawberry (Fragaria xananassa) fruits and evaluation of their utility in genetic and molecular studies , 2010, BMC Genomics.

[36]  H. Klee,et al.  Ethylene receptor degradation controls the timing of ripening in tomato fruit. , 2007, The Plant journal : for cell and molecular biology.

[37]  D. Jacob,et al.  An integrative genomics approach for deciphering the complex interactions between ascorbate metabolism and fruit growth and composition in tomato. , 2009, Comptes rendus biologies.

[38]  S. Tanksley,et al.  Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. , 2005, Journal of experimental botany.

[39]  J. Giovannoni,et al.  Genetics and control of tomato fruit ripening and quality attributes. , 2011, Annual review of genetics.

[40]  Mercedes G. López,et al.  The effects of ripening stage and processing systems on vitamin C content in sweet peppers (Capsicum annuum L.) , 2005, International journal of food sciences and nutrition.

[41]  Mark Stitt,et al.  Malate Plays a Crucial Role in Starch Metabolism, Ripening, and Soluble Solid Content of Tomato Fruit and Affects Postharvest Softening[W][OA] , 2011, Plant Cell.

[42]  M. Zanor,et al.  Systems Biology of Tomato Fruit Development: Combined Transcript, Protein, and Metabolite Analysis of Tomato Transcription Factor (nor, rin) and Ethylene Receptor (Nr) Mutants Reveals Novel Regulatory Interactions1[W][OA] , 2011, Plant Physiology.

[43]  G. Martin,et al.  Transcriptome and Selected Metabolite Analyses Reveal Multiple Points of Ethylene Control during Tomato Fruit Developmentw⃞ , 2005, The Plant Cell Online.

[44]  Alisdair R Fernie,et al.  Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[45]  J. Pech,et al.  Regulatory Features Underlying Pollination-Dependent and -Independent Tomato Fruit Set Revealed by Transcript and Primary Metabolite Profiling[W] , 2009, The Plant Cell Online.

[46]  Alessandra Devoto,et al.  Jasmonate‐regulated Arabidopsis stress signalling network , 2005 .

[47]  A. Aharoni,et al.  Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. , 2002, Journal of experimental botany.

[48]  Joachim Selbig,et al.  Robin: An Intuitive Wizard Application for R-Based Expression Microarray Quality Assessment and Analysis1[W][OA] , 2010, Plant Physiology.

[49]  R. Backhaus,et al.  Induction and Control of Chromoplast-specific Carotenoid Genes by Oxidative Stress* , 1998, The Journal of Biological Chemistry.

[50]  R. McQuinn,et al.  Integrative Transcript and Metabolite Analysis of Nutritionally Enhanced DE-ETIOLATED1 Downregulated Tomato Fruit[W] , 2010, Plant Cell.

[51]  Y. Escoufier LE TRAITEMENT DES VARIABLES VECTORIELLES , 1973 .

[52]  William Stafford Noble,et al.  How does multiple testing correction work? , 2009, Nature Biotechnology.

[53]  Fernando Carrari,et al.  Metabolic Profiling of Transgenic Tomato Plants Overexpressing Hexokinase Reveals That the Influence of Hexose Phosphorylation Diminishes during Fruit Development , 2003, Plant Physiology.

[54]  Yves Gibon,et al.  PageMan: An interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments , 2006, BMC Bioinformatics.

[55]  K. Lilley,et al.  Identification of Putative Stage-Specific Grapevine Berry Biomarkers and Omics Data Integration into Networks1[C][W][OA] , 2010, Plant Physiology.

[56]  Kashif Ali,et al.  Transcript and metabolite analysis in Trincadeira cultivar reveals novel information regarding the dynamics of grape ripening , 2011, BMC Plant Biology.

[57]  R. Wildman,et al.  Handbook of Nutraceuticals and Functional Foods , 2019 .

[58]  G. Tucker,et al.  Biochemistry of Fruit Ripening , 1993, Springer Netherlands.

[59]  P. M. Bramley,et al.  Carotenoid Biosynthesis during Tomato Fruit Development (Evidence for Tissue-Specific Gene Expression) , 1994, Plant physiology.

[60]  G. Martin,et al.  ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. , 2004, The Plant journal : for cell and molecular biology.

[61]  H. Masuda,et al.  The Role of beta-Galactosidases in the Modification of Cell Wall Components during Muskmelon Fruit Ripening. , 1992, Plant physiology.

[62]  J. Hirschberg,et al.  Carotenoid biosynthesis in flowering plants. , 2001, Current opinion in plant biology.

[63]  A. Fernie,et al.  Metabolic Profiling during Peach Fruit Development and Ripening Reveals the Metabolic Networks That Underpin Each Developmental Stage1[C][W] , 2011, Plant Physiology.

[64]  M. Zanor,et al.  Integrated Analysis of Metabolite and Transcript Levels Reveals the Metabolic Shifts That Underlie Tomato Fruit Development and Highlight Regulatory Aspects of Metabolic Network Behavior1[W] , 2006, Plant Physiology.

[65]  L. Howard,et al.  Changes in phytochemical and antioxidant activity of selected pepper cultivars (Capsicum species) as influenced by maturity. , 2000, Journal of agricultural and food chemistry.

[66]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[67]  H. Klee Control of ethylene-mediated processes in tomato at the level of receptors. , 2002, Journal of experimental botany.

[68]  J. Cushman,et al.  Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development , 2007, BMC Genomics.

[69]  Catherine Deborde,et al.  Gene and Metabolite Regulatory Network Analysis of Early Developing Fruit Tissues Highlights New Candidate Genes for the Control of Tomato Fruit Composition and Development1[C][W][OA] , 2009, Plant Physiology.

[70]  A. Mattoo,et al.  Higher polyamines restore and enhance metabolic memory in ripening fruit , 2008 .

[71]  J. Fellman,et al.  A role for jasmonates in climacteric fruit ripening , 1998, Planta.

[72]  H. Klee,et al.  The tomato ethylene receptor gene family: Form and function. , 2002, Physiologia plantarum.

[73]  Je-Gun Joung,et al.  Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. , 2012, The Plant journal : for cell and molecular biology.