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Tapetum and Middle Layer Control Male Fertility in Actinidia Deliciosa

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Tapetum and Middle Layer Control Male Fertility in Actinidia Deliciosa Annals of Botany 112: 1045–1055, 2013 doi:10.1093/aob/mct173, available online at www.aob.oxfordjournals.org Tapetum and middle layer control male fertility in Actinidia deliciosa Giuseppina Falasca1,†, Simone D’Angeli1,†, Rita Biasi2,†, Laura Fattorini1, Maja Matteucci1, Antonella Canini3 and Maria Maddalena Altamura1,* 1Department of Environmental Biology, ‘Sapienza’ University of Rome, Rome, Italy, 2Department of Science and Technologies for Agriculture, Forests, Nature and Energy, Viterbo, Tuscia University, Italy and 3Department of Biology, University of Tor Vergata, Rome, Italy * For correspondence. E-mail [email protected] †These authors contributed equally to this work Received: 28 March 2013 Returned for revision: 21 May 2013 Accepted: 13 June 2013 Published electronically: 21 August 2013 † Background and Aims Dioecism characterizes many crop species of economic value, including kiwifruit (Actinidia deliciosa). Kiwifruit male sterility occurs at the microspore stage. The cell walls of the microspores and the pollen of the male-sterile and male-fertile flowers, respectively, differ in glucose and galactose levels. In numerous plants, pollen formation involves normal functioning and degeneration timing of the tapetum, with calcium and carbohy- drates provided by the tapetum essential for male fertility. The aim of this study was to determine whether the anther wall controls male fertility in kiwifruit, providing calcium and carbohydrates to the microspores. † Methods The events occurring in the anther wall and microspores of male-fertile and male-sterile anthers were investigated by analyses of light microscopy, epifluorescence, terminal deoxynucleotidyl transferase-mediated dUTP nick-end labelling (TUNEL assay) and transmission electron microscopy coupled with electron spectroscopy. The possibility that male sterility was related to anther tissue malfunctioning with regard to calcium/glucose/galact- ose provision to the microspores was also investigated by in vitro anther culture. † Key Results Both tapetum and the middle layer showed secretory activity and both degenerated by programmed cell death (PCD), but PCD was later in male-sterile than in male-fertile anthers. Calcium accumulated in cell walls of the middle layer and tapetum and in the exine of microspores and pollen, reaching higher levels in anther wall tissues and dead microspores of male-sterile anthers. A specific supply of glucose and calcium induced normal pollen formation in in vitro-cultured anthers of the male-sterile genotype. † Conclusions The results show that male sterility in kiwifruit is induced by anther wall tissues through prolonged secretory activity caused bya delay in PCD, in the middle layer in particular. In vitro culture results support the sporo- phytic control of male fertility in kiwifruit and open the way to applications to overcome dioecism and optimize kiwi- fruit production. Key words: Actinidia deliciosa, anther, anther culture, calcium, dioecism, flower male fertility flower male sterility, glucose, middle layer, pollen, programmed cell death, tapetum. INTRODUCTION (Varkonyi-Gasic et al.,2011). In contrast with A. chinensis (Fraseretal.,2009),sexexpressioninthisspeciesstillneeds inves- Dioecism is a biological trait that characterizes many crop tigation (Varkonyi-Gasic et al.,2011). Kiwifruit clonal cultivars species of high economic value, including Actinidia deliciosa have been partially characterized by the use of RAPD and SSR (kiwifruit). Functional dioecism appears to be the dominant re- molecular markers, and some differences among the cultivars productive feature of the genus Actinidia (Ferguson, 1990). have been found; however, they do not seem to be linked to sex ex- Thus, kiwifruit exhibits clonal cultivars with flowers either pression because the genetic distance between cultivars with op- with stamens producing viable pollen and a rudimentary ovary posite sex expression may be less than that between cultivars (i.e. male-fertile clonal cultivars employed as pollen donors) or expressing the same sex (Palombi and Damiano, 2002). In withacompleteandfunctionalgynoeciumandacompleteandroe- plants with unisexual flowers, the primordia of either stamens or cium, which, however, does not produce viable pollen (i.e. male- carpels may be completely absent, e.g. in Cannabis. However, it sterileclonal cultivars employed for fruitproduction). A. deliciosa is also possible that the primordia of stamens and carpels are is a recently domesticated species, and its fruits are mostly formed in the same flower, and that inhibition of development produced by the male-sterile cultivar ‘Hayward’ following pollin- of the unwanted sex organ involves a programmed cell death ation by the male-fertile ‘Tomuri’; these are two clonal cultivars (PCD) process (Wu and Cheng, 2000). In kiwifruit, the same believed to be derived from a single seed line (Mouat, 1958; MADS-box genes as those responsible for floral organ specifica- Astridge, 1975; Zhang and Thorp, 1986). A. deliciosa is hexa tionare presentinflowers ofmale-sterileand male-fertile cultivars ploid and its genetics is difficult to investigate. Although it is (Varkonyi-Gasic et al., 2011), and arrest involving PCD at the closely related to the diploid Actinidia chinensis, A. deliciosa early microspore stage occurs in the male-sterile cultivars differs from it in many vegetative and reproductive features (Scoccianti et al., 1999; Coimbra et al.,2004). # The Author 2013. Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/ 3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1046 Falasca et al. — Sporophytic control of male fertility in kiwifruit Soluble carbohydrates provided by the anther wall sustain secretory activity, independently of anther sterility/fertility. pollen development (Engelke et al., 2010; Pacini, 2010); Degeneration occurs by PCD, but is delayed in the anther wall however, they may also be markers of male sterility, e.g. in of male-sterile flowers. High calcium signals in the tapetum tobacco (Engelke et al., 2010), sorghum (Datta et al., 2001)and and middle layer and in the microspore exine characterize cucumber (Miao et al., 2011). It has been shown that low sugar male-sterile anthers. The in vitro results show that a specific com- levels in male-sterile anthers may be related to reduced amylolytic bination of glucose and calcium ions greatly enhances pollen activity, i.e. the breakdown of starch in the stamen, as in a male- formation in male-sterile anthers. In contrast with previous sterile mutant of tomato (Bhadula and Sawhney, 1989). The results (Messina, 1993; Biasi et al., 2001), the present results aborted microspores of male-sterile kiwifruit flowers exhibit demonstrate that male fertility is controlled exclusively by the reduced glucose, galactose and galacturonic acid levels in the sporophyte in kiwifruit. cytoplasm and in the cell wall in comparison with the functional pollen of male-fertile flowers (Biasi et al.,2001). Calcium ions are known to activate and modulate many plant MATERIALS AND METHODS developmental processes, including sexual reproduction (Kong Plant material and Jia, 2004; Ge et al., 2007), but are also active during pollen androgenesis (Reynolds, 1990) and organogenesis in Anthers of the male-sterile cultivar ‘Hayward’ of Actinidia deli- vitro (Falasca et al., 2004, 2008). Most studies on the roles of ciosa var. deliciosa and of the male-fertile cultivar ‘Tomuri’ calcium in male reproduction have focused on pollen germin- were collected randomly from flowers of specimens grown in ation/tube elongation (Ge et al., 2007). However, some studies an experimental orchard of CRA-FRU (Rome, Italy). The have also demonstrated that calcium ion distribution and anthers were taken from the central flower of the inflorescence. content are related to male sterility (Tian et al., 1998; Kong In a preliminarystudy, anthers were also collected from the male- and Jia, 2004; Chen et al., 2008), carbohydrate metabolism fertile cultivar Matua (early flowering) and the male-sterile clone (Brauer et al., 1990) and signalling leading to PCD (Ning 11 (a ‘Hayward’ mutant with altered flowering time) to detect et al., 1999; Wang et al., 2001). whether the genetic differences of these genotypes (Palombi To date, there is no evidence on the effects of calcium on and Damiano, 2002) might affect the reproductive process. microsporogenesis/microgametogenesis in kiwifruit, or on a Based on the histological results (two replicates of 30 anthers possible combined effect of the ion with a specific carbohydrate each, in the same year), which showed no difference between in the control of these processes and, perhaps, in PCD. The the two male-fertile cultivars and between the two male-sterile tapetum provides carbohydrates and calcium ionsto the develop- clones, sampling was carried out by the use of ‘Hayward’ and ing microspores (Kong and Jia, 2004; Qiu et al., 2009; Engelke ‘Tomuri’ only (3 years with two biological replicates per year). et al., 2010), but also sporopollenin, necessary for exine forma- tion (Vizcay-Barrena and Wilson, 2006). The tapetum might Cyto-histological analyses have an important role in kiwifruit because aborted microspores of male-sterile anthers develop an exine and because pollen is oc- Anthers, microspores
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