THE MOLECULAR BIOLOGY ANDBIOCHEMISTRY OF FRUIT RIPENINGGRAHAM B. SEYMOUR MERVIN POOLEJAMES J. GIOVANNONIAND GREGORY A. TUCKER

THE MOLECULAR BIOLOGY AND BIOCHEMISTRY OF FRUIT RIPENINGSEYMOUR, POOLE, GIOVANNONI AND TUCKER

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ISBN: 978-0-8138-2039-2

Recent scientific advances and technological breakthroughs have revolutionized our understanding of the molecular and biochemical processes that control fruit ripening. The Molecular Biology and Biochemistry of Fruit Ripening provides a succinct yet detailed overview of the physiochemical and molecular changes in fruit that impact its quality, color, flavor, and texture.

The Molecular Biology and Biochemistry of Fruit Ripening takes a mechanistic approach that compares and contrasts ripening processes between various fruit species. An understanding of the basic mechanisms that control ripening processes can then be applied toward improvement in yield, nutritional content, and distribution. Chapters explore diverse biological aspects of the ripening process reinforced by vibrant full-color illustrations, including the evolution of fruits, the role of the plant hormone ethylene, and the biosynthesis of secondary metabolites and the structure of fruit cell walls.

Providing an essential update for this fast moving area of research, The Molecular Biology and Biochemistry of Fruit Ripening will be a valuable resource for plant and crop science researchers, crop biotechnologists, industry personnel, horticulturists, and food scientists.

EDITORS Graham B. Seymour is Professor of Plant Biotechnology and Head of the Plant and Crop Science Division at The University of Nottingham, UK.

Mervin Poole is Section Manager at Campden BRI - the UK’s largest independent membership-based organization carrying out research and development for the food and drinks industry worldwide.

James J. Giovannoni is a Research Molecular Biologist for the United States Department of Agriculture, Professor at the Boyce Thompson Institute for Plant Research and Adjunct Professor of Plant Biology at Cornell University, USA.

Gregory A. Tucker is Professor of Plant Biochemistry and Associate Dean (Science) at The University of Nottingham, UK.

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The Molecular Biology and Biochemistryof Fruit Ripening

The Molecular Biology and Biochemistryof Fruit Ripening

Edited byGRAHAM B. SEYMOUR

MERVIN POOLEJAMES J. GIOVANNONIGREGORY A. TUCKER

A John Wiley & Sons, Inc., Publication

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Contents

List of Contributors ixPreface xi

Chapter 1 Biochemistry of Fruit Ripening 1Sonia Osorio and Alisdair R. Fernie

Introduction 1Central Carbon Metabolism 4Ethylene in Ripening 7Polyamines 9Volatiles 10Cell Wall Metabolism 11Concluding Remarks 13References 13

Chapter 2 Fruit—An Angiosperm Innovation 21Sandra Knapp and Amy Litt

Introduction 21Fruit in the Fossil Record 30Fruit Variation and Angiosperm Phylogeny 32Fruit Development 33Fruit as a Driver of Angiosperm Diversity 36Acknowledgments 38References 38

Chapter 3 Ethylene and the Control of Fruit Ripening 43Don Grierson

Introduction 43Ethylene and Climacteric and Nonclimacteric Fruits 46A Molecular Explanation for System-1 and System-2 Ethylene 48Ethylene and Ripening Gene Networks in Flower and Fruit Development 53Ethylene Perception and Signaling 54Ethylene Response Factors 60

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vi CONTENTS

Ethylene and Ripening Gene Expression 60Conclusions 67Acknowledgments 68References 68

Chapter 4 Carotenoid Biosynthesis and Chlorophyll Degradation 75Peter M. Bramley

Introduction 75Distribution of Carotenoids and Chlorophylls in Fruit 75Chlorophyll Degradation and Recycling 78Carotenoids and Carotenoid Metabolites 82Future Perspectives 100Acknowledgments 102Bibliography 102

Chapter 5 Phenylpropanoid Metabolism and Biosynthesis of Anthocyanins 117Laura Jaakola

Introduction 117Cinnamic Acids 119Monolignols, Lignans, and Lignin 120Coumarins 120Stilbenoids 122Flavonoids 122Engineering Elevated Levels of Flavonoids and Other Phenylpropanoids 128Conclusion 129References 129

Chapter 6 Biosynthesis of Volatile Compounds 135Antonio Granell and Jose Luis Rambla

Introduction 135Metabolic Pathways 136Identification of Quantitative Trait Loci for Volatiles 152Metabolic Engineering of the Fruit Volatile Pathways 153Future Perspectives 154References 155

Chapter 7 Cell Wall Architecture and Metabolism in Ripening Fruit and theComplex Relationship with Softening 163Eliel Ruiz-May and Jocelyn K.C. Rose

Introduction 163Building Blocks of Fruit Cell Walls 164

CONTENTS vii

The Architecture of Fruit Cell Walls 168Cell Wall Dynamics in Ripening Fruit 171The Cuticular Cell Wall and Fruit Softening 177Summary 179Acknowledgments 180References 180

Chapter 8 Regulatory Networks Controlling Ripening 189Betsy Ampopho, Natalie Chapman, Graham B. Seymour,and James J. Giovannoni

Hormonal Control 189Genetic Networks 191Epigenetic Regulation 200References 201

Index 207

List of Contributors

Betsy Ampopho Boyce Thompson Institute for Plant Science ResearchCornell UniversityIthaca, New York, NY, USA.

Peter M Bramley School of Biological SciencesRoyal HollowayUniversity of LondonEgham, Surrey, United Kingdom.

Natalie Chapman Plant and Crop Science DivisionUniversity of NottinghamSutton Bonington, Loughborough, Leics, United Kingdom.

Alisdair R. Fernie Department of Molecular PhysiologyMax-Planck-Institute for Molecular Plant PhysiologyPotsdam-Golm, Germany.

James J Giovannoni Department of Agriculture–Agricultural Research ServiceBoyce Thompson Institute for Plant Science ResearchCornell UniversityIthaca, New York, NY, USA.

Antonio Granell Instituto de Biologıa Molecular y Celular de PlantasConsejo Superior de Investigaciones CientıficasUniversidad Politecnica de ValenciaValencia, Spain.

Don Grierson Laboratory of Molecular Physiology and BiotechnologyZhejiang UniversityZhejiang, China.

Division of Plant and Crop SciencesSchool of BiosciencesUniversity of NottinghamSutton Bonington CampusLoughborough, Leicestershire, United Kingdom.

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x LIST OF CONTRIBUTORS

Laura Jaakola Department of BiologyUniversity of OuluOulu, Finland.

Sandra Knapp Department of BotanyThe Natural History MuseumLondon, United Kingdom.

Amy Litt The New York Botanical GardenBronx, New York, NY, USA.

Sonia Osorio Max-Planck-Institute for Molecular Plant PhysiologyPotsdam-Golm, Germany.

Mervin Poole Plant Science DivisionUniversity of NottinghamSutton Bonington CampusLoughborough, Leics, United Kingdom.

Jose Luis Rambla Instituto de Biologıa Molecular y Celular de PlantasConsejo Superior de Investigaciones CientıficasUniversidad Politecnica de ValenciaValencia, Spain.

Jocelyn K.C. Rose Department of Plant BiologyCornell UniversityIthaca, New York, NY, USA.

Eliel Ruiz-May Department of Plant BiologyCornell UniversityIthaca, New York, NY, USA.

Graham B. Seymour Plant and Crop Science DivisionUniversity of NottinghamSutton BoningtonLoughborough, Leics, United Kingdom.

Gregory A. Tucker School of BiosciencesUniversity of NottinghamSutton Bonington CampusLoughborough, Leics, United Kingdom.

Preface

Evolution has fashioned multiple means of protecting seed and dispersing them upon maturation.None is as fascinating nor as consequential to humankind as the ripe and delectable fleshy fruit.Ripe fruits comprise a significant and expanding proportion of human and animal diets, whichthe medical community contends should only be increased. In addition to being visual delightswith seductive tastes and aromas, ripe fruits deliver a diverse array of antioxidants and nutrientsto those who consume them, in addition to healthy doses of carbohydrates and fiber. Thechemistry of fruits comprises attributes that producers, processors, and distributors alike seekto understand, optimize, and deliver to increasingly health-conscious consumers expecting highquality and diversity of choices. Plant scientists have endeavored to unravel the mysteries offleshy fruit biology and the underlying molecular and biochemical processes that contribute tofruit ripening and the resulting desirable attributes of fruits and fruit products.

This book offers a useful overview of fruit ontology and evolution emphasizing the exponen-tial growth in advances and discoveries in ripening-related chemistry and associated regulatoryprocesses accumulated in the last decade. The reader will appreciate the broad and deep impactof comprehensive genomics and metabolomics in addition to the computational tools neces-sary to decipher the resulting data on the progress of the field. As a consequence of theseall-encompassing approaches, fruit biology has advanced from the investigation of single genesand enzymatic reactions to the development of nuanced molecular regulatory models over-seeing complex biochemical pathways leading to numerous metabolic outputs. Looking at thephysiological and molecular symphony of events impacting textural changes of the ripeningfruit, the array of novel phenolic metabolites, or the network of genes and signaling processesregulating ethylene hormone response, it becomes strikingly clear that recent technical advanceshave moved ripening biology forward at an astounding rate. This book captures the advancesof the field and couches them in an evolutionary context and a fundamental knowledge of fruitbiology, making it an excellent primer for those interested in the field and a comprehensivereference for those familiar with it. The Molecular Biology and Biochemistry of Fruit Ripeningis essential reading for any student of plant science and those especially interested in fruitbiology and its relationship to human diet and nutrition.

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1 Biochemistry of Fruit RipeningSonia Osorio and Alisdair R. Fernie

Introduction

This chapter is intended to provide an overview of the key metabolic and regulatory pathwaysinvolved in fruit ripening, and the reader is referred to more detailed discussions of specifictopics in subsequent chapters.

The quality of fruit is determined by a wide range of desirable characteristics such asnutritional value, flavor, processing qualities, and shelf life. Fruit is an important source ofsupplementary diet, providing minerals, vitamins, fibers, and antioxidants. In particular, they aregenerally rich sources of potassium, folate, vitamins C, E, and K as well as other phytonutrientssuch as carotenoids (beta-carotene being a provitamin A) and polyphenols such as flavonols(Saltmarsh et al., 2003). A similar, but perhaps more disparate, group of nutrients is associatedwith vegetables. Thus nutritionists tend to include fruits and vegetables together as a single“food group,” and it is in this manner that their potential nutritional benefits are normallyinvestigated and reported. Over the past few decades, the increased consumption of fruitsand vegetables has been linked to a reduction in a range of chronic diseases (Buttriss, 2012).This has led the WHO to issue a recommendation for the consumption of at least 400 g offruits and vegetables per day. This in turn has prompted many countries to issue their ownrecommendations regarding the consumption of fruits and vegetables. In Britain this has givenrise to the five-a-day recommendation. A portion in the United Kingdom is deemed to be around80 g; so five-a-day corresponds to about 400 g per day. Other countries have opted for differentrecommendations (Buttriss, 2012), but all recognize the need for increased consumption.

The rationale for the five-a-day and other recommendations to increase fruit and vegetableconsumption comes from the potential link between high intake of fruits and vegetables andlow incidence of a range of diseases. There have been many studies carried out over the lastfew decades. The early studies tended to have a predominance of case-control approacheswhile recently more cohort studies, which are considered to be more robust, have been carriedout. This has given rise to many critical and systematic reviews, examining this cumulative

The Molecular Biology and Biochemistry of Fruit Ripening, First Edition.

Edited by Graham B. Seymour, Mervin Poole, James J. Giovannoni and Gregory A. Tucker.

© 2013 John Wiley & Sons, Inc. Published 2013 by John Wiley & Sons, Inc.

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