Role of plant hormones and their interplay in development and ripening of fleshy fruits
TL;DR: The new knowledge on their relative roles during tomato fruit development is evaluated with a view to understand their mechanism of action in fleshy fruits and it is envisaged that such detailed knowledge will help design new strategies for effective manipulation of fruit ripening.
Abstract: Plant hormones have been extensively studied for their roles in the regulation of various aspects of plant development. However, in the last decade important new insights have been made into their action during development and ripening, in both dry and fleshy fruits. Emerging evidence suggests that relative functions of plant hormones are not restricted to a particular stage, and a complex network of more than one plant hormone is involved in controlling various aspects of fruit development. Though some areas are extensively covered, considerable gaps in our knowledge and understanding still exist in the control of hormonal networks and crosstalk between different hormones during fruit expansion, maturation, and various other aspects of ripening. Here, we evaluate the new knowledge on their relative roles during tomato fruit development with a view to understand their mechanism of action in fleshy fruits. For a better understanding, pertinent evidences available on hormonal crosstalk during fruit development in other species are also discussed. We envisage that such detailed knowledge will help design new strategies for effective manipulation of fruit ripening.
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TL;DR: The effects of introgression or silencing of different JA- and Me-JA-related genes have been summarized in this review, which have shown a substantial role in improving crop yield and quality in different plants under stress or non-stress conditions.
Abstract: Jasmonates (JAs) [Jasmonic acid (JA) and methyl jasmonates (MeJAs)] are known to take part in various physiological processes. Exogenous application of JAs so far tested on different plants under abiotic stresses particularly salinity, drought, and temperature (low/high) conditions have proved effective in improving plant stress tolerance. However, its extent of effectiveness entirely depends on the type of plant species tested or its concentration. The effects of introgression or silencing of different JA- and Me-JA-related genes have been summarized in this review, which have shown a substantial role in improving crop yield and quality in different plants under stress or non-stress conditions. Regulation of JAs synthesis is impaired in stressed as well as unstressed plant cells/tissues, which is believed to be associated with a variety of metabolic events including signal transduction. Although, mitogen activated protein kinases (MAPKs) are important components of JA signaling and biosynthesis pathways, nitric oxide, ROS, calcium, ABA, ethylene, and salicylic acid are also important mediators of plant growth and development during JA signal transduction and synthesis. The exploration of other signaling molecules can be beneficial to examine the details of underlying molecular mechanisms of JA signal transduction. Much work is to be done in near future to find the proper answers of the questions like action of JA related metabolites, and identification of universal JA receptors etc. Complete signaling pathways involving MAPKs, CDPK, TGA, SIPK, WIPK, and WRKY transcription factors are yet to be investigated to understand the complete mechanism of action of JAs.
276 citations
Cites background from "Role of plant hormones and their in..."
...Phytohormones have a leading role in various physiological and developmental processes in plants (Rohwer and Erwin, 2008; Ashraf et al., 2010; Kumar et al., 2014)....
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TL;DR: The model for the study of fleshy fruit development is tomato, because of the availability of single gene mutants and transgenic knock-down lines, and post-transcriptional regulation by fruit-expressed microRNAs targeting several of these transcription factors.
Abstract: Fleshy fruits have evolved to be attractive to frugivores in order to enhance seed dispersal, and have become an indispensable part of the human diet. Here we review the recent advances in the understanding of transcriptional regulation of fleshy fruit development and ripening with a focus on tomato. While aspects of fruit development are probably conserved throughout the angiosperms, including the model plant Arabidopsis thaliana, it is shown that the likely orthologues of Arabidopsis genes have distinct functions in fleshy fruits. The model for the study of fleshy fruit development is tomato, because of the availability of single gene mutants and transgenic knock-down lines. In other species, our knowledge is often incomplete or absent. Tomato fruit size and shape are co-determined by transcription factors acting during formation of the ovary. Other transcription factors play a role in fruit chloroplast formation, and upon ripening impact quality aspects such as secondary metabolite content. In tomato, the transcription factors NON-RIPENING (NOR), COLORLESS NON-RIPENING (CNR), and RIPENING INHIBITOR (MADS-RIN) in concert with ethylene signalling regulate ripening, possibly in response to a developmental switch. Additional components include TOMATO AGAMOUS-LIKE1 (TAGL1), APETALA2a (AP2a), and FRUITFULL (FUL1 and FUL2). The links between this highly connected regulatory network and downstream effectors modulating colour, texture, and flavour are still relatively poorly understood. Intertwined with this network is post-transcriptional regulation by fruit-expressed microRNAs targeting several of these transcription factors. This important developmental process is also governed by changes in DNA methylation levels and possibly chromatin remodelling.
252 citations
Cites background from "Role of plant hormones and their in..."
...Ethylene signal transduction is also linked to processes controlled by other plant hormones, and this is covered elsewhere in this special issue (Kumar et al., 2014)....
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TL;DR: It is proposed that the role of apoplasmic calcium-pectin crosslinking, particularly in the xylem, is an understudied area that may have a key influence on fruit water relations and improved knowledge of the calcium-regulated signaling pathways that control ripening would assist in addressing calcium deficiency disorders and improving fruit pathogen resistance.
Abstract: Calcium has well-documented roles in plant signaling, water relations and cell wall interactions. Significant research into how calcium impacts these individual processes in various tissues has been carried out; however, the influence of calcium on fruit ripening has not been thoroughly explored. Here, we review the current state of knowledge on how calcium may impact fruit development, physical traits and disease susceptibility through facilitating developmental and stress response signaling, stabilizing membranes, influencing water relations and modifying cell wall properties through cross-linking of de-esterified pectins. We explore the involvement of calcium in hormone signaling integral to ripening and the physiological mechanisms behind common disorders that have been associated with fruit calcium deficiency (e.g. blossom end rot in tomatoes or bitter pit in apples). This review works towards an improved understanding of how the many roles of calcium interact to influence fruit ripening, and proposes future research directions to fill knowledge gaps. Specifically, we focus mostly on grapes and present a model that integrates existing knowledge around these various functions of calcium in fruit, which provides a basis for understanding the physiological impacts of sub-optimal calcium nutrition in grapes. Calcium accumulation and distribution in fruit is shown to be highly dependent on water delivery and cell wall interactions in the apoplasm. Localized calcium deficiencies observed in particular species or varieties can result from differences in xylem morphology, fruit water relations and pectin composition, and can cause leaky membranes, irregular cell wall softening, impaired hormonal signaling and aberrant fruit development. We propose that the role of apoplasmic calcium-pectin crosslinking, particularly in the xylem, is an understudied area that may have a key influence on fruit water relations. Furthermore, we believe that improved knowledge of the calcium-regulated signaling pathways that control ripening would assist in addressing calcium deficiency disorders and improving fruit pathogen resistance.
218 citations
Cites background from "Role of plant hormones and their in..."
...Fruitset and early development are triggered by auxin synthesis in the ovules during fertilization, which induces GA synthesis, reviewed in Kumar et al. (2014)....
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...The role of plant hormones in fruit development and ripening processes has been extensively reviewed (Ruan et al., 2012; McAtee et al., 2013; Osorio et al., 2013; Wang and Ruan, 2013; Kumar et al., 2014; Leng et al., 2014)....
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...GA signaling in the pericarp of Arabidopsis fruit has been demonstrated to activate a pathway degrading the growth inhibiting DELLA proteins (Fuentes et al., 2012; Kumar et al., 2014)....
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TL;DR: The present review captures the significant leads gained in the past decade in the field of plant metabolomics accompanied by a brief discussion on the current contribution and the future scope of metabolomics to accelerate plant improvement.
Abstract: Post-genomics era has witnessed the development of cutting-edge technologies that have offered cost-efficient and high-throughput ways for molecular characterization of the function of a cell or organism. Large-scale metabolite profiling assays have allowed researchers to access the global data sets of metabolites and the corresponding metabolic pathways in an unprecedented way. Recent efforts in metabolomics have been directed to improve the quality along with a major focus on yield. Importantly, an integration of metabolomics with other approaches such as quantitative genetics, transcriptomics and genetic modification has established its immense relevance to plant improvement. An effective combination of these modern approaches guide researchers to pinpoint the functional gene(s) and the characterization of massive metabolites, in order to prioritize the candidate genes for downstream analyses and ultimately, offering trait specific markers to improve commercially important traits. This in turn will improve the ability of a plant breeders by allowing them to make more informed decisions. Given this, the present review captures the significant leads gained in the past decade in the field of plant metabolomics accompanied by a brief discussion on the current contribution and the future scope of metabolomics to accelerate plant improvement.
188 citations
Cites background or result from "Role of plant hormones and their in..."
...Similar results were obtained in other agronomic crops transgenic like melon and papaya (Kumar et al., 2014)....
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...A recent work suggests cross talk between hormones during growth and development (Kumar et al., 2014)....
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References
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TL;DR: A high-quality genome sequence of domesticated tomato is presented, a draft sequence of its closest wild relative, Solanum pimpinellifolium, is compared, and the two tomato genomes are compared to each other and to the potato genome.
Abstract: Tomato (Solanum lycopersicum) is a major crop plant and a model system for fruit development. Solanum is one of the largest angiosperm genera1 and includes annual and perennial plants from diverse habitats. Here we present a high-quality genome sequence of domesticated tomato, a draft sequence of its closest wild relative, Solanum pimpinellifolium2, and compare them to each other and to the potato genome (Solanum tuberosum). The two tomato genomes show only 0.6% nucleotide divergence and signs of recent admixture, but show more than 8% divergence from potato, with nine large and several smaller inversions. In contrast to Arabidopsis, but similar to soybean, tomato and potato small RNAs map predominantly to gene-rich chromosomal regions, including gene promoters. The Solanum lineage has experienced two consecutive genome triplications: one that is ancient and shared with rosids, and a more recent one. These triplications set the stage for the neofunctionalization of genes controlling fruit characteristics, such as colour and fleshiness.
2,687 citations
"Role of plant hormones and their in..." refers background in this paper
...…crosstalk between hormonal pathways, including ethylene, auxin and ABA (Alcazar et al., 2010; Cui et al., 2010; D ow nloaded from https://academ ic.oup.com /jxb/article-abstract/65/16/4561/2877436 by guest on 20 N ovem ber 2018 Parra-Lobato and Gomez-Jimenez, 2011; Torrigiani et al., 2012)....
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TL;DR: Light is shed on the molecular basis of developmental ripening control, suggested common regulators of climacteric and nonclimacteric ripening physiology, and how these regulators affect human and animal diets.
Abstract: Fruit development and ripening are unique to plants and represent an important component of human and animal diets. Recent discoveries have shed light on the molecular basis of developmental ripening control, suggested common regulators of climacteric and nonclimacteric ripening physiology, and
1,183 citations
"Role of plant hormones and their in..." refers background in this paper
...As these changes have been observed in the context of response of various hormones, the major ripening control seems to be achieved predominantly by ethylene and ABA (Giovannoni, 2004; McAtee et al., 2013)....
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...Initial investigations on fruit ripening were mainly focused at ethylene, colour changes, and cell wall dynamics (Giovannoni, 2004; Saladie et al., 2007), whereas other ripening characteristics received less attention....
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TL;DR: It is demonstrated that an SBP-box gene is critical for normal ripening and highlights the likely importance of epialleles in plant development and the generation of natural variation.
Abstract: A major component in the regulatory network controlling fruit ripening is likely to be the gene at the tomato Colorless non-ripening (Cnr) locus. The Cnr mutation results in colorless fruits with a substantial loss of cell-to-cell adhesion. The nature of the mutation and the identity of the Cnr gene were previously unknown. Using positional cloning and virus-induced gene silencing, here we demonstrate that an SBP-box (SQUAMOSA promoter binding protein-like) gene resides at the Cnr locus. Furthermore, the Cnr phenotype results from a spontaneous epigenetic change in the SBP-box promoter. The discovery that Cnr is an epimutation was unexpected, as very few spontaneous epimutations have been described in plants. This study demonstrates that an SBP-box gene is critical for normal ripening and highlights the likely importance of epialleles in plant development and the generation of natural variation.
1,076 citations
"Role of plant hormones and their in..." refers background in this paper
...…exploration Ethylene positively regulates aroma production in melon by controlling the level of alcohol dehydrogenases (ADH), as melon fruits treated with 1-MCP and transgenic fruits with suppressed expression of the gene encoding ACC oxidase showed inhibited ADH activity (Manriquez et al., 2006)....
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TL;DR: It is illustrated that fruit development is a potentially useful system to learn more about complex regulatory mechanisms that control the division, growth, and differentiation of plant cells.
Abstract: Embryonic development in many angiosperms occurs concomitantly with the development of the ovary into a specialized organ, the fruit, which provides a suitable environment for seed maturation and often a mechanism for the dispersa1 of mature seeds, as Darwin observed. Despite centuries of intensive genetic selection of agriculturally valuable fruit, we still lack most information about how fruits develop, how this development is coordinated with embryonic development and seed formation, and the molecular, cellular, and physiological events that control fruit growth and differentiation. The last 10 years have seen a rapid surge of information on one commercially important aspect of fruit development, fruit ripening, including the genetic control of temporal events during the ripening phase (Theologis, 1992; Theologis et al., 1992). However, fewer advances have been made on temporal and spatial controls of fruit set and growth, although from the agricultura1 point of view, these aspects are of equally critical importance. We will provide a perspective on the molecular, cellular, and physiological mechanisms that must be considered as integral parts of the fruit developmental process. The discussion below will illustrate that fruit development is a potentially useful system to learn more about complex regulatory mechanisms that control the division, growth, and differentiation of plant cells.
1,035 citations
TL;DR: Gene repression and mutant complementation demonstrate that LeMADS-RIN regulates ripening, whereas LeMADS-MC affects sepal development and inflorescence determinacy, and provides molecular insight into nonhormonal regulation of ripening.
Abstract: Tomato plants harboring the ripening-inhibitor (rin) mutation yield fruits that fail to ripen. Additionally, rin plants display enlarged sepals and loss of inflorescence determinacy. Positional cloning of the rin locus revealed two tandem MADS-box genes (LeMADS-RIN and LeMADS-MC), whose expression patterns suggested roles in fruit ripening and sepal development, respectively. The rin mutation alters expression of both genes. Gene repression and mutant complementation demonstrate that LeMADS-RIN regulates ripening, whereas LeMADS-MC affects sepal development and inflorescence determinacy. LeMADS-RIN demonstrates an agriculturally important function of plant MADS-box genes and provides molecular insight into nonhormonal (developmental) regulation of ripening.
1,004 citations