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Parthenocarpic Fruit Development in Capsicum Annuum Aparna Tiwari

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Parthenocarpic Fruit Development in Capsicum Annuum Aparna Tiwari Parthenocarpic fruit development in Capsicum annuum Aparna Tiwari Thesis committee Thesis supervisor Prof.dr. Olaf van Kooten Professor of Horticultural Supply Chains, Wageningen University Thesis co-supervisors: Dr. ir. Ep Heuvelink Associate professor, Horticultural Supply Chains Group, Wageningen University Dr. Remko Offinga Associate professor, Department of Molecular and Developmental Genetics Institute of Biology, Leiden University Other members: Prof. dr. ir. P.C. Struik, Wageningen University Prof García-Martínez, Universidad Politécnica de Valência, Spain Prof.dr. G. Angenent, Wageningen University Dr. J. Haanstra, Rijk Zwaan, The Netherlands This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology and Resource Conservation. ii Parthenocarpic fruit development in Capsicum annuum Aparna Tiwari Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public onFriday 20 May 2011 at 1.30 p.m. in the Aula. iii Aparna Tiwari Parthenocarpic fruit development in Capsicumannuum Thesis, Wageningen University, Wageningen, the Netherlands (2011) With references, summaries in English and Dutch ISBN: 978-90-8585-871-3 iv Abstract Parthenocarpy (fruit set without fertilization) is a much desired trait in sweet pepper (Capsicum annuum ) production as it minimizes yield irregularity, enhances total yieldandmakes theproduction possible under suboptimal environmental conditions. Beside this, parthenocarpyimproves the commercial value of the fruitsince parthenocarpic fruits are convenient for consumption, much wanted for minimal-processed food, and possess long shelf-life.Parthenocarpy has been widely studied for tomato and Arabidopsis but not for C. annuum .Physiological and morphological characterization of parthenocarpy in C. annuum is the main focus of this thesis with emphasis on finding evidence thattomato and Arabidopsis can be used as model plants to study fruit development in C. annuum. The series of physiological and morphological changes (i.e. pollen tube growth, vascular connection between ovule and carpel, cell division and cell expansion in carpel) that occurs in a post-fertilized ovary of C. annuum was similar to that reported in tomato and Arabidopsis . Similar to these two species, C. annuum showed a hierarchy between auxin and gibberellinwhere auxin acts upstream of gibberellin in fruit set, most likely by inducing gibberellin biosynthesis.These findings indicate that fruit set mechanisms in C. annuum are similar to that reported in tomato and Arabidopsis.Parthenocarpy was evident in most of the studied genotypes of C. annuum (n=24) suggesting that somedegree of intrinsic parthenocarpy is already present in C. annuum . External application of auxin and gibberellin on the stigma of emasculated flowers enhanced parthenocarpic fruit production.GA 3 did not significantly contribute to the final fruit size. GA 3 seems to play an important role in preventing flower and fruit abscission while auxin seems to be important for both fruit set and fruit development. Almost all seedless fruits obtained either by only emasculation or emasculation followed by hormone application showed stronger growth of carpel like structures (CLS) compared to seeded fruits. Structural analogy of CLS with bel1 mutant of Arabidopsis suggests that CLS are transformed from abnormal ovules. Capsicum genotypes with high parthenocarpic potential showed a stronger CLS development suggesting a relation between female sterility and parthenocarpy. The parthenocarpic potential appeared to be controlled by a single recessive gene. The CLS phenotype and parthenocarpy could not be linked to a single locus, suggesting that absence of fertilization induces parthenocarpic fruit development and allows CLS growth, which substitutes developing seeds in promoting fruit development.This thesis provides insight in the physiology and morphology and genetic basis of parthenocarpy in C. annuum . Key words: Parthenocarpy, Capsicum , fruit set, hormones, cell division, cell expansion, auxin, gibberellin, temperature, carpel-like structures, genotype v vi Table of contents Chapter 1 General introduction 1 Chapter 2 Physiological and morphological changes during early fruit growth in Capsicum annuum 11 Chapter 3 Selection of sweet pepper ( Capsicum annuum L.) genotypes for parthenocarpic fruit growth 25 Chapter 4 Parthenocarpic potential in Sweet Pepper ( Capsicum annuum L.) is enhanced by carpel-like structures and controlled by a single recessive gene 31 Chapter 5 Auxin-induced parthenocarpic fruit set in Capsicum annuum L requires downstream gibberellin biosynthesis 59 Chapter 6 General discussion 75 References 79 Summary 93 Samenvatting 97 Acknowledgement 101 Curriculum Vitae 103 List of publications 105 PE&RC PhD Education Certificate 107 Funding 109 viii Chapter 1 General introduction Chapter 1 Introduction Sweet pepper ( Capsicum annuum L.) is an important vegetable crop worldwide. C. annuum is used as a salad, stuffing, cooked vegetable, pickled or processed and appreciated world wide for their flavor, aroma, color and as an important source of vitamin C, vitamin A (red stage), antioxidants, folic acid and fibers (Chakravarty et al. , 2009; Frank et al. , 2001; Palada et al. , 2006). Major problems experienced by sweet pepper growers are the strong week-to-week fluctuation/irregularity in yield plus the physiological disorder blossom-end- rot (BER) (Marcelis and Baan Hofman-Eijer, 1997). Irregular yield is caused by the fact that the presence of developing fruits induce flower or fruit abortion on the next few nodes (Marcelis et al. , 2004). Incidences of BER are caused by local deficiencies of calcium in young, rapidly expanding pepper fruit tissues (Bangerth, 1979; Rubio et al. , 2010). Seeds located in older fruits appear to play a dominant role in competition with flowers or fruits higher in the plant. Therefore, parthenocarpic fruits obtained by external application of auxin on the stigma of flowers results in more regular yield, minimizes the incidence of BER, improves the total yield and makes production possibleunder suboptimal environmental conditions (Heuvelink and Körner, 2001). Beside this, parthenocarpy increase the commercial value of the fruit since parthenocarpic fruits are easy to consume, much wanted for minimal-processed food, and possess high shelf-life (Gillaspy et al. , 1993; Gonzalez et al. , 2004; Habashy et al. , 2004). Despite of this, not much attention has been given to understand parthenocarpy in C. annuum. In this chapter, wesummarize the overview of various approaches that induce parthenocarpy in various crop species and possible application of each approach for inducing parthenocarpy in C. annuum is discussed. Parthenocarpy Parthenocarpy (Parthenos , virgin; karpos , fruit) is the natural or artificial induction of fruit development without pollination and fertilization. For various parthenocarpic plant varieties, an increased supply of phytohormones to the gynoecium from sources other than the developing seeds has been reported to be sufficient to induce fruit growth (Abad and Monteiro, 1989; García-Martínez, 1997; Gillaspy et al. , 1993). This observation suggests that parthenocarpic gene/s might primarily affect the hormone production, transport, and/or metabolism leading to sensitivity or higher hormone levels in the ovary capable of promoting fruit growth even in the absence of pollination and fertilization (Vivian-Smith et al. , 2001). Parthenocarpy, like stenospermocarpy and apomixis are genetically controlled traits, in which fruit set are uncoupled from the series of events that occurs after pollination and fertilization (Fig. 1).In stenospermocarpy, though distinct from parthenocarpy, normal pollination and fertilization do occur and initiate fruit development, but early embryo abortion results in seedless fruits as recorded in grapes and watermelon (Ledbetter and Ramming, 1989). Apomixis is embryo and seed development without fertilization and as a result apomictic species also produce fruit in the absence of fertilization as recorded in citrus, blackberry, 2 General Introduction mangoes and walnut (Hanna and Bashaw, 1987; Koltunow and Grossniklaus, 2003; Nybom, 1986). Fertilization Stenospermocarpy Parthenocarpy Apomixis Floral development Floral development Floral development Floral development Senescence Pollination/ Pollination/fertilization Overrule developmental arrest Overrule developmental arrest fertilization Embryo, endosperm Defect in embryo or Post-pollination floral Post-pollination floral integument growth endosperm development development development Fruit + seed Fruit development without Fruit development without Autonomous fruit and development seeds seeds seed development Figure 1 schematic representation of the developmental differences between fruit obtained by fertilization, stenospermocarpy, parthenocarpy, and apomixis. Natural occurring parthenocarpy has been identified as obligate or facultative. Genotypes with obligate parthenocarpy are unable to produce viable seeds either in the presence or in the absence of fertile pollen as reported in satsuma mandarin (George et al. ,1984). Plants with this condition are thought to be defective during female gametophyte development and require manual vegetative propagation. In contrast, facultative parthenocarpic plants
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