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A Sexual Hybrid and Autopolyploids Detected in Seed from Crosses Between Neslia Paniculata and Camelina Sativa (Brassicaceae)

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A Sexual Hybrid and Autopolyploids Detected in Seed from Crosses Between Neslia Paniculata and Camelina Sativa (Brassicaceae) Botany A sexual hybrid and autopolyploids detected in seed from crosses between Neslia paniculata and Camelina sativa (Brassicaceae) Journal: Botany Manuscript ID cjb-2019-0202.R2 Manuscript Type: Note Date Submitted by the 03-Mar-2020 Author: Complete List of Authors: Martin, Sara; Agriculture and Agri-Food Canada, Ottawa Research and Development Centre LaFlamme, Michelle; Agriculture and Agri-Food Canada, Ottawa Research and DevelopmentDraft Centre James, Tracey; Agriculture and Agri-Food Canada, Ottawa Research and Development Centre Sauder, Connie; Agriculture and Agri-Food Canada, Ottawa Research and Development Centre Brassicaceae, hybridization, autopolyploidization, neopolyploidy, gene Keyword: flow Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/botany-pubs Page 1 of 19 Botany 1 2 3 A sexual hybrid and autopolyploids detected in seed from crosses between Neslia paniculata and 4 Camelina sativa (Brassicaceae) 5 Sara L. Martin1, Michelle LaFlamme1, Tracey James1, Connie A. Sauder1 6 7 1 Agriculture and Agri-Food Canada, Ottawa Research and Development Centre, 960 Carling Ave., 8 Ottawa, Ontario, K1A 0C6 9 Corresponding Author: 10 Sara L. Martin 11 960 Carling Ave. Ottawa, Ontario, K1A 0C6 12 613-715-5406 13 [email protected] 14 15 Emails of co-authors: 16 [email protected] Draft 17 [email protected] 18 [email protected] 1 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 2 of 19 19 Abstract 20 It is important to understand the probability of hybridization and potential for introgression of 21 transgenic crop alleles into wild populations as part of pre-release risk assessment. Here we completed 22 bidirectional crosses between the emerging crop, camelina (Camelina sativa) and its weedy relative ball 23 mustard (Neslia paniculata). Ball mustard is a self-compatible annual that produces hard ball-like seeds 24 similar to canola or mustard seed in size and shape. A total of 1,593 crosses were completed and 25 collected with camelina as the maternal parent, while 3,253 crosses were successfully collected in the 26 reverse direction. Putatively hybrid seedlings were screened with flow cytometry and species-specific 27 nuclear ribosomal internal transcribed spacer (ITS) markers. Three plants had DNA contents close to 28 expectations for hybrids, but only one of these, formed on camelina, had the expected ITS markers. This 29 hybrid exhibited low fertility and neither selfDraft pollination nor backcrossing produced viable progeny. The 30 other two plants, formed on ball mustard, had high pollen and seed fertility and were identified as ball 31 mustard neoautotetraploids. Therefore, the hybridization rate between camelina and ball mustard is 32 relatively low at 1 in 20,000 ovules pollinated when camelina is the maternal parent. However, 33 autotetraploids may form frequently in ball mustard and tetraploid populations may exist in nature. 34 Key words: Brassicaceae, hybridization, autopolyploidization, neopolyploids, weeds, gene flow 2 https://mc06.manuscriptcentral.com/botany-pubs Page 3 of 19 Botany 35 Introduction 36 Within Canada, numerous plant species could receive gene flow from crops with novel traits. As 37 part of a pre-release risk assessment, it is important to understand the probability of this hybridization 38 and the potential for introgression of crop alleles into wild populations (Anderson 1949; Ellstrand and 39 Hoffman 1990; Dale et al. 1993; Warwick et al. 1999; Snow 2002; Ellstrand 2003; Messeguer 2003; 40 Devos et al. 2009). The short term fitness effects of hybridization and gene flow from crops to the wild 41 population and the long term evolutionary consequences of this introgression will depend on the 42 characteristics of the novel trait (Mallet et al. 2016). However, fundamentally, whether or not a trait can 43 be incorporated into another species’ genome, depends on the strength of reproductive isolation 44 between the lineages. This strength has proven to be highly variable across taxa with hybridity making a 45 substantial contribution to the evolutionaryDraft histories of many plant species (Mallet 2007; Abbott et al. 46 2013). 47 Camelina (Camelina sativa (L.) Crantz; n = 20 (6+7+7) is a hexaploid crop with strong potential to 48 produce high value products such as biofuel and a sustainable source of for omega-3 fatty acids for 49 human consumption (Small 2013; Berti et al. 2016). Several close relatives of camelina, including other 50 species of Camelina, Shepherd’s purse (Capsella bursa-pastoris (L.) Medik.), three species of Arabidopsis 51 (A. arenicola (Richardson ex Hooker) Al-Shehbaz, Elvin, D. F. Murray & Warwick, A. lyrata (L.) O’kane 52 &Al-Shebaz, and A. thaliana (L.) Heynhold), and ball mustard (Neslia paniculata (L.) Desv.) (Al-Shehbaz 53 and co-workers 2010; Al-Shehbaz 2012), have become naturalized in Canada and are weeds of marginal 54 and agricultural lands. Ball mustard is a self-compatible, annual or winter annual plant that, like 55 camelina, is native to central Eurasia and was first introduced into in Manitoba, Canada in the 1800s 56 (Francis and Warwick 2003). The species is generally considered diploid (n = 7) (Mulligan 1957; Al- 57 Shehbaz and co-workers 2010). 3 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 4 of 19 58 Historically, within Canada, ball mustard has been most abundant on the Canadian Prairie 59 Provinces, with occurrences recorded across the country (Francis and Warwick 2003). Ball mustard has 60 small hard ball-like seeds with strong dormancy that are able to persist in the seed bank and, because of 61 similarity in shape and size of their seeds, can be a problematic contaminant of canola (Brassica napus 62 L.) or mustard (Sinapis alba L.). Abundance of ball mustard appears to have declined from being 63 common in the 1880s (Francis and Warwick 2003) to low abundance in the Canadian Prairie Provinces in 64 the 1990s (Leeson et al. 2005). This may be a result of good control of the species with herbicides. 65 However, an Alberta population resistant to acetolactate synthase inhibitors was found in 1998 (Heap 66 2019). The genome has been sequenced (Slotte et al. 2013) and the species has received attention as a 67 system for understanding karyotype evolution in the Brassicaceae (Lysak et al. 2006; Mandáková and 68 Lysak 2008). Ball mustard is indeterminate Draftand flowers from May to September, which would overlap 69 with the flowering period of camelina. Hybridization has been reported between the two subspecies of 70 ball mustard, Neslia paniculata subsp. paniculata and the apparently hexaploid (n = 21) Neslia 71 paniculata subsp. thracica (Velen.) Bornm. (Francis and Warwick 2003; Rice et al. 2015), but we are 72 unaware of any work examining the species’ potential to make wide hybridizations. Here we performed 73 bidirectional crosses between camelina and ball mustard to establish their baseline inter-fertility. 74 Materials and Methods 75 Seed Sources 76 Five accession of camelina including both cultivated material and material collected from feral 77 populations in Canada and four accessions of ball mustard (Neslia paniculata subsp. paniculata) received 78 from botanical gardens and from material collected in Canada were used (Table 1). Seeds of ball 79 mustard had the seed coats removed prior to planting, while camelina seeds were planted directly into 80 soil, into 10 cm pots filled with a 1:2:1 mixture of soil, peat and sand. These were placed in the green 4 https://mc06.manuscriptcentral.com/botany-pubs Page 5 of 19 Botany 81 house with a 16 h photoperiod with supplemental lights programed to come on when light levels are 82 below 400 W/m2 and temperatures of 18 °C at night and 20 °C during the day. 83 Controlled Crosses 84 Three treatments were applied to each plant. Buds were emasculated and after a day were 1) 85 left un-pollinated as negative controls, 2) pollinated with self-pollen for a positive control or 3) 86 pollinated with the pollen of the other species as the crossing treatment. Further, un-manipulated 87 flowers from each plant were selected as a second positive control. As camelina has approximately 8-20 88 ovules per flower, we expected that 1000 pollinations with camelina as the maternal parent would 89 result in approximately 12,000 ovules challenged by ball mustard pollen and the power to detect 90 hybridization at a rate of 0.025% with 95% Draftconfidence (Jhala et al. 2011). In contrast, while the 91 gynoecium of ball mustard initially contains 4-6 ovules, only one, occasionally two, and more rarely, 92 three, develop into seeds. This limits the expected number of ovules/per pollination to one. As a result, 93 a thousand pollinations only results in a thousand trials for hybridity and 2,995 pollinations are required 94 for detecting a hybridization rate of 0.1% with 95% confidence (Jhala et al. 2011). Any seed that formed 95 on flowers that received foreign pollen were treated like the seeds of their maternal parent and grown 96 under the same conditions. 97 Hybrid Screening 98 Flow cytometry was used to screen putative hybrids between ball mustard and camelina based 99 on their DNA content following protocols described previously (Martin et al. 2015, 2017). Briefly, 100 samples were fresh leaf material from rosettes that were collected in the greenhouse and placed on ice, 101 chopped with a new, sharp razor blade in Galbraith buffer (0.75 mL), and then kept in the dark while 102 they stained for 30– 40 min with propidium iodide. Samples were run with radish (Raphanus sativus L. 103 ‘Saxa’ (1.11pg/2C)) as an external standard for initial screening, however camelina was used as an 5 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 6 of 19 104 internal standard for precise DNA estimates with three technical replicates completed over three 105 different days (Doležel et al.
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