Molecular and morphological phylogenetic analysis of Brachiaria and Urochloa (Poaceae)
Introduction
Brachiaria (Trin.) Griseb. and Urochloa P. Beauv. sensu Clayton and Renvoize (1986) belong to the tribe Paniceae, subfamily Panicoideae of the Poaceae family. Brachiaria, a pantropical genus contains about 100 species mainly from the Old World, is found in a wide range of habitats from semi-desert to swamp. Urochloa is also a paleotropical genus including 12 species mainly from African savannahs.
Some species formerly belonging to Brachiaria but now placed in Urochloa are well known as forage grass or cereal crops. Among these, B. deflexa (=U. deflexa) is cultivated in West Africa, while B. ramosa (=U. ramosa) is cultivated in south India (Kimata et al., 2000, Porteres, 1976). Some African species of Brachiaria have been introduced into the Americas as pasture grasses, such as B. plantaginea and B. mutica (Parsons, 1972); both species are now Urochloa. Five species of Brachiaria, all of which are now in Urochloa, that have been released as commercial cultivars in different tropical American countries (Keller-Grein et al., 1996) are Urochloa, i.e., U. brizantha, U. decumbens, U. dictyoneura, U. humidicola, and U. ruziziensis (Table 1).
Currently, the genus Brachiaria (Trin.) Griseb. is the most widely used forage grass in the South American savannas due to its physiological tolerance to low-fertility acid soils of the tropics (Rao et al., 1996). There are seven germplasm collections of Brachiaria and Urochloa in ex situ conservation in the world. All together they hold almost 1000 distinct accessions of 33 species (Keller-Grein et al., 1996). Despite the economic importance of Brachiaria and Urochloa their taxonomic positions remain unclear.
Clayton and Renvoize (1986) describe Brachiaria as an annual or perennial grass with an inflorescence of racemes along a central filiform to ribbon-like rachis. The spikelets are single or paired, sessile or pedicelled, as well as adaxial and plump. Sometimes the lowest internode is elongated forming a short cylindrical stipe. The lower glume is mostly shorter than the spikelet, but sometimes almost equal in length to the spikelet. The upper lemma is obtuse to acute and occasionally mucronate. Likewise, they describe Urochloa as an annual or perennial grass with inflorescence of racemes along an axis. The spikelets are single or paired, abaxial, plano-convex, and cuspidate to acuminate. The lower glume is shorter than the spikelet, except in U. paspaloides. The upper lemma is mostly obtuse with a long mucro with exceptions occurring in U. platyrrhachis (emucronate) and U. rudis (acuminate).
Taxonomically Brachiaria has had various ranks over time. Trinius (1826) described Brachiaria as a section of the genus Panicum and circumscribed the section by its racemose primary branches. Grisebach (1853) elevated Brachiaria to generic level because of this trait.
Subsequently, Nash (1903) defined Brachiaria by the presence of a transverse rugose upper floret and adaxial spikelets. Stapf (1920) used the racemose primary branches as a diagnostic character to transfer several species from Panicum to Brachiaria. Since then most taxonomists have adopted the adaxial orientation of the spikelet and the racemose primary branches as most important characters to separate the species of Brachiaria from those of other genera.
Beauvois (1812) published Urochloa with U. panicoides as type species. Hughes (1923), Stapf (1920), and Henrard (1941) used the traits spikelet mucronate or aristulate and their abaxial position to transfer several species from Panicum to Urochloa.
Several authors have discussed the weakness of the characters used to separate Brachiaria from Urochloa (Morrone and Zuloaga, 1992, Morrone and Zuloaga, 1993, Webster, 1987, Webster, 1988). They argue that the spikelet orientation used to distinguish Brachiaria (adaxial, with the first glume turned toward the rachis) from Urochloa (abaxial, with the first glume opposite to the rachis) works only for single spikelets on primary branches. When the spikelets are paired, however, both genera have adaxial orientation.
Webster (1987) states that the secondary character used to distinguish these genera, presence or absence of an awned upper floret, has continuous variation from apiculate to mucronate in both genera. This is not a discrete character and therefore has limited use for defining these genera.
Floristic studies conducted in Vietnam (Nguyen, 1966), in Australia (Webster, 1987), in North America (Webster, 1988, Zuloaga and Morrone, 2003), in South America and Mexico and Central America (Morrone and Zuloaga, 1992, Morrone and Zuloaga, 1993), and in Malaysia (Veldkamp, 1996b, Veldkamp, 2004) have over time recircumscribed species of Brachiaria into Urochloa. On the other hand, several species not included in these floristic studies have been transferred to Urochloa (Davidse, 1993, López-Ferrari and Espejo Serna, 2000, Morrone and Zuloaga, 1991, Nelson and Fernández, 1998, Wunderlin and Hansen, 2001). In contrast, Sharp and Simon (2002) maintain the name Brachiaria for all species that occur in Australia and have been transferred to Urochloa by Webster (1987), until a cladistic survey has been done for the whole tribe. Additionally, some authors do not agree to transfer the annuals species of Brachiaria to Urochloa (Veldkamp, 1996a, Webster, 1987, Zuloaga and Morrone, 2003). Recently, Veldkamp (2004) transferred these annuals species from Brachiaria to the new genus Moorochloa (M. eruciformis, M. malacodes, and M. schoenfelderi).
Studies of the leaf-blade anatomy in Paniceae (Hattersley and Watson, 1976, Renvoize, 1986, Thompson and Estes, 1986) have found that certain species of the genera Brachiaria, Eriochloa, and Urochloa belong to the C4, PS(PCK) photosynthetic pathway. Ogundipe and Olatunji (1992) in a study of West African species of Brachiaria found variation in the C4 subtype. Most species were of Kranz MS; however, a minority were of Kranz PS.
By using anthecial epidermis micromorphology, Thompson and Estes (1986) grouped the genus Brachiaria into nine patterns, which are not discrete but form a network from unadorned to highly ornamented surface patterns. This study also revealed a high level of variability and inter-gradation between the genera Brachiaria, Eriochloa, and Urochloa.
Renvoize et al. (1996) reviewed the genus on a global scale to understand the morphological variation. A total of 97 species of Brachiaria from Africa, America, Asia, and Australia were placed in nine morphological groups using nine primary characters and eight secondary characters based on inflorescence and spikelet features (Table 2).
A phylogenetic reconstruction based on morphological ramification traits determined Brachiaria and Urochloa to be paraphyletic genera. The monophyletic group composed by Brachiaria, Urochloa, Eriochloa, Thuarea, Yvesia, and Eccoptocarpha is supported by the synapomorphies photosynthetic pathway PS(PCK) and the adaxial orientation of the lower glume and mucro in the upper spikelet (Frank, 1998).
Phylogenetic work using molecular data on these genera is in its infancy. To test potentially competing hypotheses of generic relationships for Brachiaria and Urochloa, one molecular dataset using the internal transcribed spacer (ITS) region and a morphological data set were constructed.
The ITS region of nuclear ribosomal DNA has been used in grasses at different taxonomic levels. The rate of nucleotide substitutions in the ITS region is useful for evaluation of generic and species level relationships, as shown by the phylogenetic analysis of Sorghum (Sun et al., 1994) and Zea (Buckler and Holtsford, 1996). Because of the small size of the region (fewer than 700 base pairs (bp)) and adequate variation (numerous point mutations and indels events), this gene was selected for use in a phylogenetic analysis of the subfamily Pooideae (Hsiao et al., 1994, Hsiao et al., 1995).
The ITS region was used in this project to examine the phylogenetic relationship among species of the genera Brachiaria and Urochloa. This region has been widely used in molecular systematic studies at lower taxonomic levels because spacer sequences evolve rapidly and can therefore resolve lower level relationships better than slowly evolving genes such as 18S or rbcL (Baldwin et al., 1995, Soltis et al., 1993).
Section snippets
Preparation and sampling
Twenty-two species of Brachiaria and Urochloa were included in the study. Two species were chosen from Urochloa sensu Clayton and Renvoize (1986), U. mosambicensis, and U. trichopus. A total of 19 species of Brachiaria were chosen from the informal morphological grouping of Renvoize et al. (1996), representing six of the nine groups (Table 2). Thirteen of these 19 species previous to the study of Renvoize et al. (1996) had been transferred to Urochloa: U. arrecta, U. brizantha, U. comata, U.
Molecular data
The length of the region containing ITS1, 5.8S, and ITS2 of the 22 Brachiaria and Urochloa species varied from 582 nucleotides, in U. decumbens, to 587 nucleotides, in B. dura, U. eruciformis, U. xantholeuca, U. ruziziensis, and U. mosambicensis. The ITS1 region ranged from 202 to 207 bp and the ITS2 region ranged from 214 to 218 bp. The 5.8S subunit was 164 bp in length in all species. Most of the variation was found in the spacers while the 5.8S subunit had only a few point mutations and no
Discussion
The independent and combined topologies found that species of Urochloa are grouped in strongly supported clades with species of Brachiaria, Eriochloa, and Melinis. The analyses therefore suggest that Urochloa–Brachiaria as a complex is paraphyletic with Eriochloa and Melinis.
The high number of unambiguous synapomorphies from the nucleotide sites of the ITS region (rDNA) indicate a strong affinity between Urochloa, Brachiaria, Eriochloa, and Melinis. In addition, there was one morphological
Acknowledgments
The authors thank Brigitte Maass from International Livestock Research Institute, Ethiopia, and Claudia Guevara from International Centre for Tropical Agriculture, Colombia, for the shipment of the samples leaves. Steve Renvoize from the Royal Botanic Gardens, Kew, for his contribution on morphological data. Daniel Debouck, John Miles from International Centre for Tropical Agriculture, Colombia, and Elizabeth A. Kellogg from University of Missouri for helpful comments made to the contents of
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