The Potential for Crop to Wild Hybridization in Eggplant
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American Journal of Botany 102 ( 1 ): 129 – 139 , 2015 . T HE POTENTIAL FOR CROP TO WILD HYBRIDIZATION IN EGGPLANT ( S OLANUM MELONGENA ; SOLANACEAE) 1 IN SOUTHERN INDIA P RIYA D AVIDAR 2 , A LLISON A . S NOW 3,6 , M UTHU R AJKUMAR 2 , R EMY P ASQUET 4 , M ARIE-CHRISTINE D AUNAY 5 , AND E VANS M UTEGI 3 2 Department of Ecology and Environmental Sciences, Pondicherry University, Kalapet, Pondicherry 605014, India; 3 Department of Evolution, Ecology, and Organismal Biology, Ohio State University, 318 W. 12th Avenue, Columbus, Ohio 43210 USA; 4 IRD, UR 072, LEGS 91198 Gif-sur-yvette, France; Université Paris-Sud 11 91400 Orsay, France; and 5 INRA, Unité de Génétique & Amélioration des Fruits et Légumes, UR1052, Domaine St Maurice, CS 60094 F-84143 Montfavet cedex, France • Premise of the study: In India and elsewhere, transgenic Bt eggplant ( Solanum melongena ) has been developed to reduce insect herbivore damage, but published studies of the potential for pollen-mediated, crop- to- wild gene fl ow are scant. This informa- tion is useful for risk assessments as well as in situ conservation strategies for wild germplasm. • Methods: In 2010–2014, we surveyed 23 populations of wild/weedy eggplant ( Solanum insanum ; known as wild brinjal), car- ried out hand-pollination experiments, and observed pollinators to assess the potential for crop- to- wild gene fl ow in southern India. • Key results: Wild brinjal is a spiny, low-growing perennial commonly found in disturbed sites such as roadsides, wastelands, and sparsely vegetated areas near villages and agricultural fi elds. Fourteen of the 23 wild populations in our study occurred within 0.5 km of cultivated brinjal and at least nine fl owered in synchrony with the crop. Hand crosses between wild and cul- tivated brinjal resulted in seed set and viable F1 progeny. Wild brinjal fl owers that were bagged to exclude pollinators did not set fruit, and fruit set from manual self-pollination was low. The exserted stigmas of wild brinjal are likely to promote outcross- ing. The most effective pollinators appeared to be bees ( Amegilla , Xylocopa , Nomia , and Heterotrigona spp.), which also were observed foraging for pollen on crop brinjal. • Conclusion: Our fi ndings suggest that hybridization is possible between cultivated and wild brinjal in southern India. Thus, as part of the risk assessment process, we assume that transgenes from the crop could spread to wild brinjal populations that occur nearby. Key words: brinjal; crop–wild hybridization; fl owering times; genetic resources; India; pollinator observations; seed set; Solanum insanum ; transgenic; wild eggplant; wild germplasm. Worldwide, governmental regulatory agencies typically re- and Wainwright, 2008 ). Many crops are known to exchange quire information about the extent to which a transgenic crop will genes with wild, weedy, or feral relatives, including rice, canola, hybridize with its wild or weedy relatives (e.g., Pilson and squash, sorghum, papaya, sunfl ower, alfalfa, beet, carrot, lettuce, Prendeville, 2004 ; Marvier and Van Acker, 2005 ). This informa- creeping bentgrass, and other species (e.g., Ellstrand, 2003 ; tion is used to determine whether transgenes may spread to un- Stewart et al., 2003 ; Ellstrand et al., 2013 ). Indeed, the commer- managed populations of the crop’s wild relatives and, if so, cialization of transgenic crops over the past two decades has whether the transgenes could persist and cause any unwanted triggered a large number of studies on the extent to which each outcomes (e.g., transferring herbicide resistance to agricultural crop species can contribute genes to neighboring populations of weeds; Lu and Snow, 2005 ). In addition, various stakeholders wild/weedy relatives (e.g., Ellstrand et al., 2013 ). When the po- have an interest in knowing whether transgenes are likely to tential for crop-to-wild gene fl ow has been established, further spread from crop to crop, crop to weeds, and crop to wild rela- research has been carried out to determine how novel transgenic tives for legal, ethical, and philosophical reasons (e.g., Mercer traits, such as resistance to insect herbivores or pathogens, affect the fi tness of recipient plant genotypes (e.g., Burke and Rieseberg, 1 Manuscript received 13 September 2014; revision accepted 1 December 2003 ; Snow et al., 2003 ; Sasu et al., 2009 ). 2014. To date, only a few commercialized transgenic crop species The authors thank the Lillian Goldman Charitable Trust for funding this have the potential to exchange genes with neighboring wild, research; H. Ponniah, S. Carr, M. Islam Najar, A. Rahim, and R. Lekshmi weedy, or feral populations. These include canola (Brassica na- for help with the fi eldwork; S. Puyravaud and H. Ponniah for photography; pu s), rice ( Oryza sativa ), and squash ( Cucurbita pepo ), and in D. Palik for statistical analyses; and J.-P. Puyravaud for creating the map in each case, research was carried out to understand the potential Fig. 1 and other logistical assistance. They also thank D. Palik, H. Chang, for gene fl ow (e.g., Ellstrand et al., 2013 ). The situation is quite and A. Maassen for helpful comments on the manuscript and R. Nayar for different for eggplant ( Solanum melongena ; Solanaceae). Ef- voucher specimen numbers. This project was undertaken as part of a memorandum of understanding between Pondicherry University and Ohio forts to develop transgenic eggplant in India have been under- State University. way for more than a decade ( Padmanaban, 2009 ), and Bt 6 Author for correspondence (e-mail: [email protected]) eggplant with lepidopteran resistance recently was approved for commercial release in Bangladesh ( Chakraborty, 2014 ). doi:10.3732/ajb.1400404 However, few peer-reviewed papers address the potential for American Journal of Botany 102 ( 1 ): 129 – 139 , 2015 ; http://www.amjbot.org/ © 2015 Botanical Society of America 129 130 AMERICAN JOURNAL OF BOTANY [Vol. 102 transgenes to spread to unmanaged populations of wild or poricidal anthers that shed pollen profusely when “buzzed” by bees, as is typi- weedy relatives of this crop, which is known locally as brinjal cal of many species in the Solanaceae (e.g., Buchmann and Hurley, 1978 ). In- (this common name is used below). To our knowledge, the dividual plants produce hermaphroditic (bisexual) fl owers with stigmas that extend beyond the anthers, as well as fl owers with a rudimentary ovary that are present study is the fi rst to show that extant populations of wild functionally male (referred to as “male” later). Likewise, in many crop acces- relatives can occur near cultivated brinjal and are likely to hy- sions of brinjal, fl owers at the base of the infl orescence are more likely to set bridize with the crop due to cross pollination by native bees. fruit, whereas more distal fl owers are functionally male ( Pradeepa, 2002 ). The Initially, Bt brinjal was promoted by the United States fruits of wild brinjal are fl eshy, bitter, multiseeded, obovoid or round, and typi- Agency for International Development (USAID) and others for cally become golden orange-yellow at maturity. Fruits can be processed and deployment in India, where yields of cultivated brinjal are often used for food and Ayurvedic medicinal treatments (e.g., Kudlu and Stone, 2013 ). The seeds are probably dispersed by domestic livestock and wild verte- diminished by lepidopteran damage ( Choudhary and Gaur, brates, as well as people. 2009 ; Padmanaban, 2009 ). The regulatory status of Bt brinjal in India is currently uncertain following a 2010 moratorium on its Study region — Our study focused on the Western Ghats region, which is a release and a great deal of controversy over its safety for human mountainous escarpment covering about 160 000 km 2 , running parallel to the consumption and the environment ( Jayaraman, 2010 ; Choudhary west coast of India from about 8 ° N to 21 ° N latitude. This region has been rec- et al., 2014 ). Before the moratorium, the Indian Report of the ognized as a biodiversity hotspot due to high levels of endemic and threatened Expert Committee ( EC-II, 2009 ) examined the potential for species ( Myers, 1990 ). It represents an important in situ repository of germ- gene fl ow from Bt brinjal to various wild and weedy relatives plasm for cultivated plants, particularly spices, and is considered to be the cen- ter of origin for black pepper, Piper nigrum ( Joy et al., 2007 ; Pandey et al., and concluded that such gene fl ow is unlikely. In addition, the 2008 ). The elevation of this area ranges from near sea level to ~2500 masl. report stated that “no instances of natural interspecifi c hybrid- Rainfall seasonality increases from south to north, infl uencing vegetation types ization with wild species have been reported for cultivated brin- ( Pascal, 1988 ) and tree diversity ( Davidar et al., 2005 ). The South West “sum- jal” ( EC-II, 2009 , p. 35). However, the scientifi c literature mer” monsoon brings rain to the southern coastline of Kerala around May and shows that several wild Solanum species have been used as June and then moves northward; it retreats in reverse. Later, the North East or germplasm in breeding programs to improve cultivated brinjal “winter” monsoon brings rain to the eastern fl ank of the Western Ghats during the months of October to December and is restricted to southern areas. (e.g., Venkataramani, 1946 ; references in Mutegi et al., 2015 ), and putative crop–wild hybrids have been observed in the fi eld ( Viswanathan, 1975 ; Karihaloo et al., 1995 ). Studies of the ge- Distribution, fl owering phenology, and proximity to cultivated brinjal — netic diversity of cultivated and wild brinjal accessions also We studied wild brinjal populations at 23 sites located on private lands within 12 administrative districts and three states of southern India ( Table 1 , Fig. 1 ). The suggest that crop–wild hybridization may have occurred in the sites were chosen based on accessibility and our goal of including a large geo- past ( Karihaloo et al., 1995 ; Knapp et al., 2013 ; Mutegi et al., graphic area, spanning about 600 km from north to south.