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Assisted-Selection of Naturally Caffeine-Free Coffee Cultivars—Characterization of Snps from a Methyltransferase Gene

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Assisted-Selection of Naturally Caffeine-Free Coffee Cultivars—Characterization of Snps from a Methyltransferase Gene Mol Breeding (2017) 37:31 DOI 10.1007/s11032-017-0636-6 Assisted-selection of naturally caffeine-free coffee cultivars—characterization of SNPs from a methyltransferase gene Patrícia Favoretto & Carla Cristina da Silva & Aline Gomes Tavares & Gabriela Giatti & Patrícia Favoretto Moraes & Mary Tulia Vargas Lobato & Maria Bernadete Silvarolla & Guerreiro Oliveiro-Filho & Mirian Perez Maluf Received: 30 June 2016 /Accepted: 7 February 2017 # Springer Science+Business Media Dordrecht 2017 Abstract Breeding of caffeine-free coffee cultivars re- significant association between presence of selected quire tools for an early selection of progenies bearing SNPs and reduced caffeine content. Moreover, this as- this later trait. Genes from caffeine synthesis and degra- sociation occurs through all evaluated genetic back- dation represent major targets for the development of grounds and generations, indicating an inheritance sta- molecular markers for assisted selection. In this study, bility of both trait and markers. The molecular markers we characterized SNPs identified on the caffeine syn- described here represent a successful case of assisted- thase gene from AC1 mutant, a naturally caffeine-free selection in coffee, indicating their potential use for arabica coffee plant. Molecular analysis of normal and breeding of caffeine-free cultivars. mutant sequences indicates the occurrence of SNPs in protein domains, potentially associated with caffeine Keywords Assisted-selection . Caffeine content . synthesis in coffee. Progenies F2,F1BC1 and BC from Caffeine synthase . Coffee . Molecular markers crosses of AC mutants and elite cultivars were evaluated regarding caffeine content in grains and genomic segre- gation profile of selected SNPs. Genotyping analysis Introduction allowed the discrimination between homozygous and heterozygous plants. Quantification of caffeine content Caffeine is a widely known and investigated compound indicated a significant variability among progenies and a from coffee grains, due to its effects on both human low frequency of caffeine-free plants. Statistical analy- health and on coffee plants physiology. As some of ses of genotyping and phenotyping results showed those effects upon human health are not desirable, breeding programs worldwide pursue the development of naturally caffeine-free cultivars, while retaining other Electronic supplementary material The online version of this article (doi:10.1007/s11032-017-0636-6) contains supplementary sensorial and quality attributes. material, which is available to authorized users. Caffeine content, on most of Coffea arabica cultivars is : : : : around 1% (percentage of dry weigh), and C. canephora P. Favoretto A. G. Tavares G. Giatti P. F. Moraes cultivars have around 2%. One known variety of M. T. V. Lobato : M. B. Silvarolla : G. Oliveiro-Filho : M. P. Maluf (*) C. arabica with low caffeine content is laurina,with EMBRAPA and Coffee Center Agronomic Institute/ IAC, around 0.6% of caffeine in fruits (Tango and Carvalho, Campinas, Brazil 1963). Other Coffea species, however, exhibited a lower e-mail: [email protected] caffeine content in grains, such as C. dewevrei (1.0%), C. C. da Silva C. eugenioides (0.4%), C. salvatrix (0.7%), and Molecular Biology and Genetic Engineering Center/UNICAMP, C. racemosa (0.8%) (Mazzafera and Carvalho 1992). In Campinas, Brazil addition, species such as C. pseudozangebariae and 31 Page 2 of 10 Mol Breeding (2017) 37:31 C. richardii have no caffeine in grains (Campa et al. The selection of naturally caffeine-free plants in seg- 2005). Studies demonstrated that absolute content of caf- regating populations is an arduous task. High selection feine results from a balance between synthesis and degra- cost, limited effectiveness of analytical methods for caf- dation. Activity quantification of biosynthetic enzyme feine content and specially the long juvenile period using radioactive compounds characterized caffeine con- associated with a poor correlation between levels detect- tent of several C. arabica varieties, including the mutant ed in leaves and grains are major challenges for breeders. laurina (Mazzafera et al. 1994). The authors concluded Molecular markers have been used with success for that the rates of caffeine synthesis and degradation in assisted selection in several plant species, and then grains change during fruit maturation and among could aid to overcome difficulties on selection of low cultivars. In other similar study, Ashihara and Crozier caffeine coffee progenies. Therefore, we tested several (1999) demonstrated that low caffeine levels in polymorphisms observed on mutant caffeine synthase C. eugenioides result from a slow synthesis associated gene for their potential use as molecular markers in the with a rapid degradation. coffee breeding program. Among those, we validated One breeding strategy to develop low caffeine coffee two neighbor SNPs in progenies F2 and F1BC1,from cultivars is to transfer this trait from Coffea species to crosses involving AC mutants and elite C. arabica cul- C. arabica. However, this strategy was unsuccessful due tivars. The validation comprised SNPs genotyping and to limitations on inter-specific crosses (Charrier 1978; phenotyping regarding caffeine content of individual Mazzafera and Carvalho 1992). In another strategy, plants. These analyses indicated a high correlation be- Silvarolla et al. (2000) focused on the natural variability tween genotype and phenotype, and demonstrated the of caffeine content in C. arabica wild accessions col- potential of those SNP markers to select caffeine-free lected at Ethiopia. Caffeine quantification on grains plants. revealed a variability directly associated with geograph- ical origin (Silvarolla et al. 2000). Later, Silvarolla et al. (2004) identified three plants (namely AC1, AC2 and Material and methods AC3) with an average content of 0.076%, which opened the perspective for a naturally caffeine-free coffee culti- Plant material var. Despite the lack of caffeine, grains from AC1 have a similar chemical composition and overall cup quality as Coffee plants have different origin and belong to the those of regular coffee (Benatti et al. 2012, Silvarolla, IAC Coffea Germplasm Collection, Campinas, Brazil unpublished results). In this context, crosses between (Table 1). The C. arabica accesions AC1, AC2, and accession AC1 and cultivar Mundo Novo (MN) initiat- AC3 have reduced levels of caffeine. Elite C. arabica ed a breeding program aiming to transfer the low caf- cultivars Mundo Novo (MN IAC 376–4), Catuaí feine trait to elite cultivars. Vermelho (CV 81 and CV 144), IAC Ouro Verde Molecular analyses of AC1 revealed several aspects (OV), Bourbom Vermelho (BV IAC), and Obatã (OB that affect the transfer of low caffeine trait. Benatti et al. IAC 1669–20) have regular caffeine content. Selected (2012) verified that AC1 fruits are smaller than fruits progenies from reciprocal crosses between ACs and from MN, and have reduced activity of theobromine elite cultivars, F2 from both open pollination and self- synthase and caffeine synthase. Expression analyses pollination, and progenies from diverse F2 and back- indicated that in AC1 fruits exhibited a lower accumu- crosses have variable caffeine content. Table 1 shows lation of transcripts from genes encoding those methyl- detailed information regarding plant identity, origin, and transferases compared to normal MN fruits (Maluf et al. caffeine content. Young mature leaves of each plant 2009). Besides this, the genomic sequence of caffeine were collected and maintained at -80 °C for DNA synthase gene from AC1 revealed several nucleotide extraction. polymorphisms, including a base substitution that re- sults in a replacement of a valine for an isoleucine at the In silico analyses enzyme active site (Maluf et al. 2009). Thus, the low caffeine content of AC1 plants results from a combina- For identification of single-nucleotide polymorphisms tion of a reduced gene expression and a possible knock- (SNPs) GeneBank sequences of caffeine synthase CCS1 out mutation of caffeine synthase. (AB086414) and CaDMXT1 (AB084125) were aligned Mol Breeding (2017) 37:31 Page 3 of 10 31 Table 1 Origin of evaluated germplasm with corresponding caffeine content in grains Genotypes Origin Description Caffeine AC1 Turrialba introduction Acession Traces AC2 Turrialba introduction Acession Very low to regular AC3 Turrialba introduction Acession Low to regular C. arabica Mundo Novo IAC 376–4 C. arabica Sumatra X Cultivar Regular C. arabica Bourbon Vermelho C.arabica Catuaí Vermelho IAC 81 C. arabica Caturra Amarelo X Cultivar Regular C. arabica Mundo Novo C. arabica Catuaí Vermelho IAC 144 C. arabica Caturra Amarelo X Cultivar Regular C. arabica Mundo Novo C. arabica Ouro Verde IAC H 5010–5 C.arabica Catuaí Amarelo IACH2077–2–12-70 X Cultivar Regular C. arabica Mundo Novo IAC 515–20 C. arabica Obatã Vermelho IAC 1669–20 C. arabica Villa Sarchi (CIFC H 361) X Cultivar Regular Híbrido de Timor (CIFC 832/2) Bourbon Vermelho Bourbon introduction Cultivar Regular with genomic sequences from C. arabica cv Mundo Genotyping was performed by quantitative PCR Novo (MN) and AC1 using the software BioEdit using a combination of primers and specific MGB (Maluf et al. 2009). Genomic sequences were amplified TaqMan probes (Life Technologies). Caffeine synthase by PCR using gene specific primers designed upon specific primers and fluorescent probes annealing to a available caffeine synthase sequences at the time. Two region with two SNPs
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