Nicotiana gandarela Augsten & Stehmann (Solanaceae), sp. nov., a small ’tobacco’ known only from one locality at Serra do Gandarela, in the state of Minas Gerais, Brazil, is described and illustrated. It is morphologically characterized by its rosulate basal leaves, red corolla with a short tube not inflated at the apex, and the peculiar habitat, a shaded site under a rocky outcrop ledge along a forested stream. Phylogenetic analyses based on a combined dataset of nuclear (ITS) and plastid (ndhF, trnLF, and trnSG) DNA sequences revealed that the species belongs to the Nicotiana sect. Alatae and is sister to the clade with the remaining species in the section. A key for the identification of Brazilian species of the section is given. The unusual habitat, the small population size, and the intense pressure of mining activities in the surroundings made the species assessed as Critically Endangered (CR), needing conservation efforts to avoid its extinction.

Endemism, IUCN, Minas Gerais, mining, molecular phylogeny

Nicotiana L. is a Solanaceae genus known mostly because of tobacco (N. tabacum L.), a crop cultivated worldwide, but its diversity goes further. It is the fifth-largest genus in the family, with 82 species (Knapp 2020). Nicotiana occurs in South America and Australia, with one species from Africa (Namibia). The Andean region is recognized as the center of diversity of the group in the Americas, as for many other clades in Solanaceae (Goodspeed 1954; Dupin et al. 2017). Molecular phylogenies are available for the genus (Aoki and Ito 2000; Chase et al. 2003; Clarkson et al. 2004; Clarkson et al. 2017), and sectional revision is provided based on phylogenetic analyses, indicating 13 sections (Knapp et al. 2004).

In Brazil, the known native species belong to the Nicotiana sect. Alatae Goodsp. (hereafter Alatae). This section is morphologically characterized by herbaceous habit, rosulate and sessile leaves, usually viscid pubescent, few leaves on upper stems, and an abrupt dilatation at the throat of the corolla tube (Knapp et al. 2004). The section comprises two cytogenetic groups: one displays chromosome number 2n = 20 and includes two species, N. longiflora Cav. and N. plumbaginifolia Viv., distributed from Argentina to the USA; the other presents chromosome number 2n = 18 and includes N. alata Link & Otto, N. bonariensis Lehm., N. forgetiana Hemsl., N. langsdorffii Weinm., N. mutabilis Stehmann & Semir and N. azambujae L. B. Sm. & Downs, occurring in Brazil, Argentina, Uruguay, and Paraguay (Goodspeed 1954; Clarkson et al. 2004; Knapp et al. 2004). The internal phylogenetic relationships of the section are still not well resolved, with the two groups recovered as sisters (Clarkson et al. 2004) or with the 2n = 18 group as paraphyletic (Clarkson et al. 2017). According to the plastid or nuclear markers used for the reconstruction, section diversification is proposed between 6.2 Ma and 7.7 Ma, respectively (Clarkson et al. 2017).

Nicotiana can be considered a taxonomically well-studied genus for the Brazilian flora (Vignoli-Silva and Mentz 2005; Vignoli-Silva and Stehmann 2020), in which six native, N. alata, N. bonariensis, N. langsdorffii, N. forgetiana, N. mutabilis, and N. azambujae, and two naturalized species, N. tabacum, and N. glauca Graham, are recognized. Morphometric analyses based on the corolla size and shape of N. forgetiana throughout its geographical distribution showed that the species seems to include two distinct taxonomic groups, one not yet formally described (Teixeira et al. 2021). Among the Brazilian species, only N. mutabilis is considered endangered (Vulnerable) because of its small geographic distribution and just a few known populations (Stehmann et al. 2002; CNCFlora [http://cncflora.jbrj.gov.br/portal/pt-br/profile/Nicotiana%20mutabilis]). Nicotiana azambujae needs further investigation, as it is only known from the type collection.

Within Brazil, the Southern region holds the largest number of Nicotiana species, which inhabit ecotonal environments between the grasslands and the Araucaria forest (Mixed Ombrophilous Forest) in the Atlantic Forest domain (Teixeira et al. 1986; Overbeck et al. 2007). This is an important biogeographic area for several taxa that have their evolutionary history related to this vegetation mosaic (Iganci et al. 2011; Fregonezi et al. 2013). Species richness decreases towards the north, with N. bonariensis being the species with the northern-most distribution, reaching the grasslands at the high altitude regions of the Mantiqueira Range (Minas Gerais and Rio de Janeiro states) and the Espinhaço Range (Minas Gerais and Bahia states).

During floristic studies in the Quadrilátero Ferrífero, a mountainous area with large mineral reserves in Minas Gerais, with significant biological importance and high anthropic pressures (Drummond et al. 2005; Jacobi et al. 2011), samples of a small Nicotiana specimen with red flowers were collected. As the phenotype matched with none of the known Nicotiana species from Brazil, we assumed it could be a new species. In this work, we test this hypothesis using morphological and molecular data.

Overall, the recovered phylogenetic relationships were similar to those previously obtained (Chase et al. 2003; Clarkson et al. 2004; Knapp et al. 2004; Clarkson et al. 2017). Phylogenetic trees generated showed that the samples collected in the Serra da Gandarela in Minas Gerais are genetically distinct from all known species of Nicotiana used in our analyses. Nicotiana gandarela was recovered as the sister of all other species belonging to the Alatae (both of the groups with distinct cytotypes, 2n = 18 and 2n = 20; Clarkson et al. 2004; Knapp et al. 2004). The internal nodes of the group 2n = 18 showed low support, and the lack of chromosome accounts to the new species does not permit any inferences about the phylogenetic relationships within the section.

The new species is an annual plant, with rosulate leaves, long-attenuate to the base, sessile, viscid-pubescent, and a zygomorphic corolla, all morphological traits associated with the species of the Alatae (Knapp et al. 2004). The decurrent leaf bases on the stem and the abrupt dilatation at the corolla throat, commonly found in the other species of the section (Goodspeed 1954), are lacking in the new species. The habit resembles that of N. bonariensis because of its rosulate leaves and scapose inflorescence. However, N. gandarela differs from N. bonariensis in its ombrophilous and extremely narrowly distributed habitat, its diurnal anthesis with red corollas with tube < 15 mm long, rather than being being heliophilous, widespread, with nocturnal anthesis, and white corollas with a tube usually > 15 mm long.

Corolla color is variable in the Alatae, including white, yellow, pink, magenta, and purple-red. Such variation reflects an evolutionary history of radiation to distinct pollinator agents (Ippolito et al. 2004; Kaczorowski et al. 2005; Knapp 2010). Red flowers are usually associated with bird pollination (Faegri and van der Pijl 1979), and hummingbirds were already reported pollinating N. forgetiana, a pink to purple-red flowered species distributed in southern Brazil (Ippolito et al. 2004). Empirical data on the effective pollinator of N. gandarela are still necessary.

The Quadrilátero Ferrífero in Minas Gerais is located in the southern Espinhaço Range, a mountainous chain where the Cerrado (tropical Savannah) and Brazilian Atlantic Forest, two hotspots of biodiversity, connect (Mittermeier et al. 2004). The vegetation is a mosaic of topologies and vegetation, including grasslands, savannah, and forests (Spósito and Stehmann 2006), whose distributions are influenced by an altitudinal gradient, ranging from about 700 m to 2,080 m (Borges et al. 2011). In the region, besides the new species, a further two species of the Alatae are found, N. bonariensis and N. langsdorffii. The first usually inhabits the grasslands at higher altitudes known as Campos Rupestres (Silveira et al. 2016), while the second is generally associated with disturbed areas. Both grow mainly in open and sunny sites, as with most species of the Alatae, and the peculiar, shaded habitat of N. gandarela seems to be unique in the section. The microhabitat of the new species roughly resembles that of Petunia exserta Stehmann, an endemic species from Rio Grande do Sul, in Southern Brazil, but where the geology and vegetational matrix are totally different (Lorenz-Lemke et al. 2006; Stehmann et al. 2009). In both cases, few or no species share the ground where these two species grow, meaning that they are fragile, with low, competitive capacity, but are presumably adapted to survive in these empty niches. Penumbral plant communities have also been described for the Campos Rupestres in Minas Gerais, where several species were reported as growing in small caves (Alves and Kolbek 1993), but until now, no Solanaceae species have been registered in these areas.

The new species deserves special conservation attention because it inhabits a small and rare habitat, if not unique, in the Quadrilátero Ferrífero, a region that is suffering intensive habitat loss (Salles et al. 2018) and has been the scenario of recurrent environmental disasters (Carmo et al. 2017; Rotta et al. 2019). Floristic inventories looking for new populations should be carried out in the surrounding forested areas, including the Serra do Gandarela National Park, following the drainage lines in the valleys. Also, we suggest the engagement of local people in trying to find other populations because of the impossibility of looking for similar areas since they are hidden by forest in satellite images. In the end, although we emphasize that the species should be primarily preserved in its natural habitat, ex-situ conservation measures might also be necessary (CNCFlora 2016) in order to prevent its extinction.

We thank the Coordination for the Improvement of Higher Education Personnel – Brazil (CAPES) –Financing Code 001 and FAPEMIG for the scholarship to MA and CNPQ (APQ 306086/2017–4) for financial support to JRS. Thanks also to the Center for Microscopy at the Universidade Federal de Minas Gerais (http://www.microscopia.ufmg.br) for providing the equipment and technical support for experiments involving electron microscopy. We thank the reviewers of the work for their valuable suggestions. And, especially, we thank Miss Gloria Regina Perpétuo for kindly allowing collections on her property.