Horticultural Reviews, Volume 47

Ian Warrington

• Publisher: Wiley
• Year: 2019
• Print ISBN: 9781119625339
• eBook ISBN: 9781119625346
• Edition: 1
• Topic: Ciencias biológicas
• Subtopic: Horticultura

Horticultural Reviews presents state-of-the-art reviews on topics in horticultural science and technology covering both basic and applied research. Topics covered include the horticulture of fruits, vegetables, nut crops, and ornamentals. These review articles, written by world authorities, bridge the gap between the specialized researcher and the broader community of horticultural scientists and teachers.

1
Molecular Physiology of Fruit Growth in Apple

Anish Malladi

Department of Horticulture, University of Georgia, Athens, GA, USA

ABSTRACT

Fruit growth and development are processes of primary biological importance and of considerable commercial significance. In apple, the fleshy fruit is derived largely from non‐ovarian tissue. Regulation of fruit growth in apple is therefore likely distinct from that in other model fleshy fruit species. Fruit growth is an integration of multiple processes that are regulated through developmental factors, phytohormones, and availability of metabolic resources. These factors differentially influence growth during diverse stages of development, and across different tissues within the fruit. In recent years, substantial progress has been made in identifying some of the major molecular components and mechanisms involved in the regulation of apple fruit growth. This review presents a comprehensive analysis of our current knowledge of the molecular physiology of fruit growth in apple and identifies gaps where future research is needed to expand our knowledge of the regulation of this trait.

KEYWORDS: cell division; cell expansion; fruit development; fruit size; organ growth

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1. INTRODUCTION
2. MORPHOLOGY AND ANATOMY OF THE APPLE FRUIT
3. FLOWER GROWTH BEFORE BLOOM
4. FRUIT SET
5. FRUIT GROWTH
   1. Components of Fruit Growth: Cell Production, Expansion, and Void Spaces
   2. Fruit Growth and its Regulation
   3. Cell Production Related Genes and Regulation of Fruit Growth
   4. Organ Size Related Genes and Regulation of Fruit Growth
   5. Floral Homeotic Genes and Regulation of Fruit Growth
   6. Cell Wall Modifying Genes and Regulation of Fruit Growth
   7. Metabolism and Regulation of Fruit Growth
   8. Phytohormones and the Regulation of Fruit Growth
   9. A Note on the Measurement of Growth
6. CONCLUSIONS

LITERATURE CITED

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I. INTRODUCTION

Apple (Malus × domestica) is one of the most widely grown temperate fruit crops in the world. Fruit growth and development are not only of botanical significance but are also of vast economic significance in apple production. In this review, growth is defined as the increase in size of the organ, while development is defined as the progression of the organ through various phenological stages. The main emphasis of this review is on the processes and factors mediating fruit growth. However, often, growth of an organ and the processes that mediate it are intimately associated with its development. Hence, where applicable, these inter‐relationships will also be discussed.

II. MORPHOLOGY AND ANATOMY OF THE APPLE FRUIT

The apple fruit is botanically a “pome.” Fruits of this class are characterized by the presence of fleshy exocarp and mesocarp tissues and a cartilaginous endocarp. The majority of the fruit tissue is comprised of accessory tissue (Pratt 1988). The central region of an apple fruit is typically constituted by five locules that are derived from five carpels from a syncarpous ovary. Each of these carpels may contain up to four ovules which upon fertilization can yield one to four seeds (Pratt 1988). The seeds are surrounded by the cartilaginous endocarp tissue at maturity. A ring of five sepal and five petal vascular traces occurs towards the periphery of the locules and is often referred to as being the core‐line. Tissue outside of this core‐line develops into the major fleshy and economically significant part of the apple fruit (Figure 1.1). At maturity, this tissue may constitute over 80% of the fruit volume (Tukey and Young 1942; Goffinet et al. 1995).

Ontogeny of the fleshy region of the fruit outside of the core‐line and the precise localization of ovarian tissue inside of it have been debated extensively and reviewed previously (Pratt 1988). Briefly, two conflicting hypotheses have been proposed to explain the ontogeny of fruit tissues. According to MacDaniels (1940), the receptacular hypothesis indicates that the major fleshy region of the fruit is derived from axial tissues. The central region of the fruit extends from the pedicel into the fruit and the outer fleshy tissue represents an extension of the cortical region peripheral to the vascular tissue within the stem. Hence, this tissue is referred to as the cortex (Figure 1.1). As an extension of this terminology, tissue inside of the core‐line (vascular tissue) is referred to as the pith. The location of the ovarian tissues is within the pith region and restricted to cell layers immediately surrounding the locules (Figure 1.1). Further, the true fruit is composed of five drupe‐like structures characterized by a cartilaginous endocarp. As the cell layers constituted by the exocarp and mesocarp tissues are few, most of the pith is comprised of parenchymatous cells of non‐ovarian origin. The alternative appendicular hypothesis presents a divergent view. In this context, the tissue peripheral to the core‐line originates from the fusion of the basal tissues of appendages: multiple floral organs including the petals, sepals, and stamens (MacDaniels 1940). Hence, this tissue is often described as a floral tube or a hypanthium derived from fused basal regions of floral appendages. Tissue inside of the core‐line is considered of ovarian origin, such that the innermost layer of this tissue is the endocarp while the rest is constituted by fleshy exocarp and mesocarp tissues. The core‐line is regarded as the line of fusion between the floral tube and the ovary. The relative merits of each of these theories have been evaluated with many recent authors preferring the appendicular hypothesis (Pratt 1988), largely owing to interpretations from comparative vascular anatomies across Rosaceae family fruits, as elegantly described by MacDaniels (1940), as well as data from cytochimeras summarized by Pratt (1988). Very few studies since the 1950s have addressed the origin of these tissues, despite its botanical significance.

Figure 1.1 Transverse section of the apple fruit displaying the primary tissues. *: The fleshy pericarp here is shown to indicate interpretation of the fruit morphology according to the receptacular hypothesis. According to this interpretation, tissue immediately surrounding the locule constitutes the pericarp. The appendicular hypothesis considers tissue inside of the core‐line to be of ovarian origin as described in the text.

An effective way to determine the origin of these tissues in the apple fruit is through the application of specific tissue‐based markers for development. As the fruit and some of its constituent parts are derived from specific floral organs, identification of markers defining these floral organs in the fruit tissues, especially during early fruit development, can provide clues to the origin of these tissues. The ABC model describes development of floral organ identity (Bowman et al. 1991; Coen and Meyerowitz 1991) and has been extensively validated across many plant systems (Bowman et al. 2012; Irish 2017). According to this model, members of the A class of gene products determine sepal identity, and in interaction with those of the B class gene products, the identity of petals. Interaction of the B and C class gene products influences stamen development, while the C class gene products regulate gynoecium development (Irish 2017). Putative homologs of these classes of genes, many of which are MADS box transcription factors, have been identified in apple. The apple APETALA2 (AP2) is a putative A class gene, the transcripts for which were shown to be abundant in sepal tissues (Kotoda et al. 2000) and in the cortex/floral tube region during early fruit development (Yao et al. 1999). This suggested that the fleshy region of the apple fruit was likely derived at least from sepal tissues. Further, facultatively parthenocarpic spontaneous mutants of apple, ‘Rae Ime’ and ‘Spencer Seedless’ were identified to be defective in one type of B class genes, PISTILLATA (PI; Yao et al. 2001). Transcript accumulation of the PI gene was abundant within the petals but could not be observed in the cortex/floral tube region of the developing apple fruit at four weeks after bloom (Yao et al. 2001, 2018). These data suggested that petal and stamen tissues did not likely contribute substantially to development of the cortex/floral tube region of the fruit. The A class gene defining sepal identity, AP2, is regulated post‐transcriptionally by microRNA 172 (miR172). In apple, miR172 has been associated recently with regulation of fruit growth and final size (Yao et al. 2015). Higher levels of miR172 were associated with a reduction in fruit growth while the opposite was true under lower levels of miR172. Overexpression of miR172p (one of several active miR172) in transgenic ‘Royal Gala’ plants resulted in a dramatic reduction in fruit size (Yao et al. 2015). The authors proposed that the cortex/floral tube was largely derived from the base of the sepals and post‐transcriptional alteration of the A class gene product, AP2, in these transgenic plants leads to altered growth of tissue derived from this floral organ. Together, these data strongly support the appendicular theory of apple fruit development and suggest that the basal regions of the floral organs, particularly the sepals, contribute greatly to development of the major fleshy tissue of the apple fruit. There are, however, a few limitations to the above approaches. Many of the genes described above have been identified and described in apple as floral organ identity genes that have clearly defined roles during flower development, but their roles in post‐flowering fruit development are not as well characterized (Yao et al. 2016). While their transcript and protein accumulation in specific parts of the flower would be clearly indicative of organ identity, the significance of such accumulation at later stages and during fruit growth may need to be interpreted with caution. Further, in case of miR172, substantial growth and development of the fruit cortex/floral tube tissue was still noted as the hypanthium in transgenic lines, where it was overexpressed, was reduced by only about 25% during early fruit development (Yao et al. 2015). Presumably, basal regions of the petals and stamens may still contribute to the growth and development of this tissue. The current availability of additional floral tissue identity genes and newer approaches that aid in isolat...

Table of contents

• Cover
• Table of Contents
• Contributors
• Dedication: Theodore DeJong
• 1 Molecular Physiology of Fruit Growth in Apple
• 2 Mechanosensing of Plants
• 3 Microgreens: Microgreens: Definitions, Product Types, and Production Practices
• 4 The Durian: Botany, Horticulture, and Utilization
• 5 The genus Cupressus L.: Mythology to Biotechnology with Emphasis on Mediterranean Cypress (Cupressus sempervirens L.)
• 6 Taxonomy and Botany of the Caricaceae
• 7 Entomopathogens: Potential to Control Thrips in Avocado, with Special Reference to Beauveria bassiana
• Subject Index
• Cumulative Subject Index
• Cumulative Contributor Index
• End User License Agreement