Services on Demand
Print version ISSN 0001-3765
An. Acad. Bras. Ciênc. vol.83 no.3 Rio de Janeiro Sept. 2011 Epub July 15, 2011
Beatriz Appezzato-da-GlóriaI; Graziela CuryII
IDepartamento de Ciências Biológicas, Escola Superior de Agricultura 'Luiz de Queiroz', Universidade de São Paulo, Caixa Postal 09, 13418-900 Piracicaba, SP, Brasil
IIDepartamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 277, Cidade Universitária, Butantã, 05508-090 São Paulo, SP, Brasil
In the Brazilian Cerrado (neotropical savanna), the development of bud-bearing underground systems as adaptive structures to fire and dry periods can comprise an important source of buds for this ecosystem, as already demonstrated in the Brazilian Campos grasslands and North American prairies. Asteraceae species from both woody and herbaceous strata have subterranean organs that accumulate carbohydrates, reinforcing the adaptive strategy of these plants to different environmental conditions. This study aims to analyse the morpho-anatomy of underground systems of six species of Asteraceae (Mikania cordifolia L.f. Willd., Mikania sessilifolia DC, Trixis nobilis (Vell.) Katinas, Pterocaulon alopecuroides (Lam.) DC., Vernonia elegans Gardner and Vernonia megapotamica Spreng.), to describe these structures and to verify the occurrence and origin of shoot buds, and to analyse the presence of reserve substances. Individuals sampled in Cerrado areas in São Paulo State showed thick underground bud-bearing organs, with adventitious or lateral roots and presence of fructans. Xylopodium was found in all studied species, except for Trixis nobilis, which had stem tuber. The presence of fructans as reserve, and the capacity of structures in the formation of buds indicate the potential of herbaceous species of Asteraceae in forming a viable bud bank for vegetation regeneration in the Brazilian Cerrado.
Key words: anatomy, buds, Compositae, fructans, stem tuber, xylopodium.
No Cerrado brasileiro (savana neotropical), o desenvolvimento de sistemas subterrâneos que produzem gemas, como estruturas adaptativas contra o fogo e períodos de seca, pode compreender um importante suprimento de gemas para esse ecossistema, como já demonstrado nos campos brasileiros e nas pradarias norte-americanas. Espécies de Asteraceae tanto do estrato lenhoso, quanto do herbáceo têm órgãos que acumulam carboidratos, reforçando a estratégia adaptativa dessas plantas a diferentes condições ambientais. Este estudo tem o objetivo de analisar a morfo-anatomia de sistemas subterrâneos de seis espécies de Asteraceae (Mikania cordifolia L.f. Willd., Mikania sessilifolia DC, Trixis nobilis (Vell.) Katinas, Pterocaulon alopecuroides (Lam.) DC., Vernonia elegans Gardner e Vernonia megapotamica Spreng.), para descrever essas estruturas e verificar a ocorrência e origem de gemas caulinares, e analisar a presença de substâncias de reserva. Indivíduos amostrados em áreas de Cerrado no Estado de São Paulo apresentaram órgãos subterrâneos espessados produtores de gemas, com raízes adventícias ou laterais e presença de frutanos. Em todas as espécies estudadas foi constatada a presença de xilopódio, com exceção de Trixis nobilis, a qual apresentou caule tuberoso. A presença de frutanos como reserva e a capacidade de estruturas na formação de gemas indicam o potencial de espécies herbáceas de Asteraceae em formar um banco de gemas viável para regeneração da vegetação no Cerrado brasileiro.
Palavras-chave: anatomia, gemas, Compositae, frutanos, caule tuberoso, xilopódio.
The Cerrado vegetation is composed of a mosaic with different physiognomies due to distinct factors, such as deep and well drained soils that are acidic and with high aluminium content, seasonality, with dry periods of 3-4 months, and fire (Coutinho 1982). Species from the herbaceous strata are dominant in open physiognomies ("campos", grasslands). Plants have seasonal growth: the aboveground biomass dies during autumn, and these species persist as thick underground systems (Filgueiras 2002). During spring and the beginning of rainy season, individuals rapidly resprout and flower using the reserves stored in the underground structures. Alonso and Machado (2007) and Appezzato-da-Glória et al. (2008a) suggested that bud-bearing underground systems could contribute to the formation of a belowground bud bank in the Cerrado. Bud bank was first described by Harper (1977), and its concept was expanded by Klimesova and Klimes (2007). It comprises all buds from plants, which can be potentially used for vegetative regeneration by the formation of new shoots after the partial or total removal of aboveground parts caused by extreme climatic factors as drought or fire. Recently, the importance of underground systems of the bud bank for the regeneration of vegetation after disturbance and on the maintenance of plant populations were described by some authors for the subtropical grasslands in Southern Brazil ("Campos grasslands" by Fidelis 2008) and the North American prairies (Benson et al. 2004, Dalgleish 2007).
Among the different types of underground systems found in the Cerrado, some can be classified as xylopodium (Hayashi and Appezzato-da-Glória 2007, Appezzato-da-Glória et al. 2008a), tuberous roots, stemlike or radicular difuse system (Alonso and Machado 2007) and rhizophores (Hayashi and Appezzato-da-Glória 2005). The presence of such organs can influence the population dynamics of plant species, since they are able to produce new shoots after the removal of aboveground biomass. According to Kauffman et al. (1994), fire can stimulate the formation of new shoots from buds located in underground organs in the Cerrado, being thus an important trait for plant persistence after disturbance events (Soares et al. 2006). Recurrent fires can favour especially species with higher capacity of resprouting. After fires, there is an increase in number of species resprouting from buds located in underground organs after the death of aboveground biomass, confirming thus the importance of such bud-bearing organs (Medeiros and Miranda 2008, Fidelis 2008).
Verdaguer and Ojeda (2005) associated the importance of the bud bank and the carbohydrate reserves. Reserves of carbohydrates decreased in underground organs during the resprouting phase, as observed by Carvalho and Dietrich (1993) and Portes and Carvalho (2006). According to Hoffmann (1999), in woody species of Cerrado, plants invest in carbohydrates accumulation in underground storage organs, which allow them to rapidly recover after biomass loss caused by fire and assuring, thus, their survival.
Asteraceae plays an important role on the herbaceous and woody vegetation of Cerrado (Almeida et al. 2005). Several species have thick underground structures with storage reserves, mostly fructans, and a high capacity of bud formation (Tertuliano and Figueiredo-Ribeiro 1993). Fructans are not only sources of carbon, but they also play an important role for plants in environments with water restriction due to their rapid polymerization and depolymerization reactions involved in osmoregulation processes (Nelson and Spollen 1987, Pontis 1989, Hendry 1993, Figueiredo-Ribeiro 1993, Talbott and Zeiger 1998, Orthen 2001).
Therefore, this study aims to analyse the underground systems of six species of Asteraceae (Mikania cordifolia L.f. Willd., Mikania sessilifolia DC, Trixis nobilis (Vell.) Katinas, Pterocaulon alopecuroides (Lam.) DC., Vernonia elegans Gardner and Vernonia megapotamica Spreng.) describing their different structural types, verifying the occurrence and origin of shoot buds and, finally, analyzing the presence of reserve substances.
MATERIALS AND METHODS
The species of this study (Mikania cordifolia, Mikania sessilifolia, Trixis nobilis, Pterocaulon alopecuroides, Vernonia elegans and Vernonia megapotamica) were selected from surveys in the state of São Paulo (Tertuliano and Figueiredo-Ribeiro 1993, Katinas 1996, Almeida et al. 2005, Ishara et al. 2008), and the criteria of selection was analyzing species of the same genera (in the case of Mikania and Vernonia) and among different genera (Mikania, Pterocaulon, Vernonia and Trixis), and compare the subterranean systems types among them. Adult individuals were collected in natural populations in areas of Cerrado located in Botucatu (22°53"S, 8°29"W) and Itirapina (22°13"S, 47°54"W), São Paulo State, Brazil, where Asteraceae is well represented. The vouchers of the specimens (88792, 88791, 92159, 88790, 88787 and 88789, respectively) are deposited in the ESA Herbarium, Brazil.
For the anatomical study, underground systems of three adult plants were fixed in FAA 50 (1 part formaldehyde: 1 part glacial acetic acid: 18 parts 50% ethanol, v/v) for 48 h (Johansen 1940), dehydrated in a graded ethylic series and infiltrated in glycol methacrylate resin (Leica Historesin-LeicaTM - Wetzlar, Germany). Serial sections (5-7μm thick) were performed on a rotary microtome and stained with toluidine blue O (Sakai 1973). Freehand cross-sections were also cut and stained with astra blue and basic fuchsin and, subsequently, dehydrated in a graded ethylic series, and 50 and 100% butyl acetate, respectively. Permanent slides were embedded in synthetic resin. The presence of phenolic compounds was investigated in sections from fresh or plastic resin-embedded samples using ferric trichloride (Johansen 1940).
To identify the fructans of the inulin-type, samples of subterranean structures were fixed in 70% ethanol and sectioned by freehand. Inulin crystals were visualised under polarised light, and the presence of these crystals was confirmed by a treatment with thymolsulphuric acid reagent (Johansen 1940).
Photomicrographs were taken with a Nikon Labophot microscope or a Nikon SMZ-2T stereomicroscope. The images were digitally captured with a Leica DMLB microscope (LeicaTM - Wetzlar, Germany) by using a video camera plugged to a computer utilising the IM50 (LeicaTM - Wetzlar, Germany) software for image analysis.
All studied species (Fig. 1a-h) had thickened and bud-bearing underground systems (Table I), with or without thickened roots. Additionally, all species accumulated fructans of inulin-type in the parenchyma of adventitious roots (Fig. 2a), except for Trixis nobilis, which also showed fructan accumulation in the thickened underground structure, and Pterocaulon alopecuroides, which accumulates only in the thickened underground structure (Table I).
Based on our anatomical study, we classified T. nobilis as a stem tuber (Fig. 1e), and the thickened woody axis of underground systems of M. cordifolia, M. sessilifolia, P. alopecuroides, V. elegans and V. megapotamica as a xylopodium (Fig. 1b-d, 1f-h).
The size and shape of xylopodia varied among species (Fig. 1), but a common feature is the self-grafting of the stems basis formed in different development periods (Fig. 2b, 3a, b). Buds could be found spread all over the structure, protected by cataphylls (Fig. 2c), or they were concentrated in the median part of the organ in Pterocaulon alopecuroides. Buds originating from the cambium of xylopodia could be observed in M. cordifolia, M. sessilifolia, P. alopecuroides and V. elegans (Fig. 3d, e). Buds located at the upper portion of the stem tuber of Trixis nobilis and on the xylopodium of Vernonia megapotamica were axillaries (Fig. 3a, c).
The xylopodia of M. cordifolia, M. sessilifolia, V. elegans and V. megapotamica were of stem-like origin, which was confirmed by the centrifugal development of the primary xylem (Fig. 3f). The xylopodium of Pterocaulon alopecuroides, on the other hand, was a radicular structure (Fig. 3g).
In all xylopodia analysed, the 2-4 cortical parenchyma cell layers containing phenolic compounds functioned as a protective tissue (Fig. 4a). The cover tissue of stem tuber of Trixis nobilis consisted of epidermis with stomata and trichomes (Fig. 4b). Brachisclereids in the cortex could be observed in all the studie species. In Vernonia elegans and V. megapotamica, prismatic crystals were found in the brachisclereids (Fig. 4c). The underground stem-like axis of Trixis nobilis showed cortical vascular bundles (Fig. 4d).
Mikania cordifolia, the only liana species (Fig. 1a), had a xylopodium with vascular cylinder characterised by the formation of successive layers of secondary phloem, cambium and secondary xylem, with abundant conjunctive tissue (Fig. 5a, c). Mikania sessilifolia and the other studied species, which are plants with erect habitus, showed vascular cylinders with secondary phloem, cambium and secondary xylem (Fig. 5b).
The presence of thickened and bud-bearing underground systems, distributed superficially in the driest portion of the soil in the Cerrado, verified in all studied species, indicates their importance in storing water and nutrients needed for aboveground sprouting during the rainy season (Rizzini and Heringer 1961, Appezzato-da-Glória et al. 2008a). In the Cerrado species, the importance of fructan reserves in underground structures, as verified in the studied species, is mostly related to regeneration processes of aboveground biomass, flowering and plant resistance against water loss (Figueiredo-Ribeiro 1993, Portes and Carvalho 2006, Itaya et al. 2007). Dias-Tagliacozzo et al. (2004) demonstrated that the resistance of Vernonia herbacea (Vell.) Rusby (Asteraceae) to water deficit is regarded to alterations in the metabolism of fructans, hich favoured the water retention in the rhizophores. In experiments carried out with Viguiera discolor Baker (Asteraceae), Isejima et al. (1991) pointed out that flowering induced individuals to produce a higher content of fructans in tuberous roots than in control plants. Carvalho and Dietrich (1993) also verified that Vernonia herbacea, during the vegetative and dormant phases, achieved the highest levels of fructan concentration in underground organs. On the other hand, during the flowering and sprouting phases, the levels of fructan decreased (Figueiredo- Ribeiro et al. 1991).
Xylopodium, as described here for most species, is a common underground organ, being found in more than 90 genera in some Brazilian Biomes (Appezzato-da-Glória et al. 2008a). This structure was described by Lindman (1900) for an underground system that is very common in grasslands of the southern part of Brazil and in the Cerrado Biome, and found more often in plants in areas under frequent influence of fires than in excluded ones (Fidelis 2008). According to Rizzini (1965), it is a perennial thickened woody organ with numerous buds and high resprout capacity, formed from tuberisation of the hypocotyl or the root-stem transition region and of the proximal portion of the main root. Its structure, ontogenesis and ecological function do not found correspondence with previously subterranean structures described in the international literature, but this term is already accepted by Botanists from other countries who had the opportunity to study Brazilian vegetation, and some Brazilian authors have already employed the term in other studies (Alonso and Machado 2007, Appezzato-da-Glória et al. 2008a, Cury and Appezzato-da-Glória 2009). The variation of the xylopodium size and shape verified in the present study was already mentioned by Appezzato-da-Glória et al. (2008a) for Asteraceae species of the Cerrado. Xylopodium buds of cambial origin, as observed in M. cordifolia, M. sessilifolia, P. alopecuroides and V. elegans, was also reported by Vilhalva and Appezzato-da-Glória (2006) and Appezzato-da-Glória et al. (2008a). Plants with the presence of xylopodia showed seasonal growth and, besides the loss of aboveground biomass during the dry season or destruction caused by e.g. fire, the bases of aboveground shoots and their buds persisted. Therefore, at the upper portion of the xylopodia, stems formed in different development periods naturally graft; moreover, in this portion, buds are axillary like in Vernonia megapotamica. The production of stems periodically leading to the formation of a self-grafting structure on the bases of the stem axes is a common feature for xylopodia (Paviani 1987). This phenomenon increases the complexity of this organ and the number of available buds for sprouting. Therefore, xylopodia play an important role on the survival and regeneration of the Cerrado species, bearing several viable buds for plant resprouting after disturbance events.
The anatomical structure of xylopodia can be radicular, stem-like or both, depending on the analysed species (Appezzato-da-Glória et al. 2008a). The stemlike origin of xylopodium, as described in M. cordifolia, M. sessilifolia, V. elegans and V. mepapotamica, has already been observed for some other species, such as Isostigma megapotamicum (Spreng.) Sherff (Asteraceae) (Vilhalva and Appezzato-da-Glória 2006); radicular origin, as described in Pterocaulon alopecuroides, was observed for Clitoria guyanensis (Aubl.) Benth (Leguminosae) (Rizzini and Heringer 1961). The protective tissue, constituted by parenchyma cells filled with phenolic compounds, found in all xylopodia analysed, was also described in rhizomes of Rhaponticum carthamoides (Asteraceae) by Lotocka and Geszprych (2004). The presence of phenols in these layers is related to the protection against external biotic and abiotic agents (Hutzler et al. 1998). The covering tissue of stem tuber of Trixis nobilis consisted of epidermis with stomata and trichomes. Such traits were also described for rhizophores of Smilax quinquenervia Vell. (Smilacaceae) by Andreata and Menezes (1999), Vernonia herbacea and V. platensis (Hayashi and Appezzato-da-Glória 2005), and Orthoppapus angustifolius (Appezzato-da-Glória et al. 2008b). As already proposed by Andreata and Menezes (1999), the presence of stomata and trichomes, including secretory trichomes (Appezzato-da-Glória et al. 2008b) in underground stem-like systems, suggests the evolution of these stems from an aerial ancestral structure.
Brachysclereids present in the cortex of all studies species regards the sclerophylly common in the Cerrado plants (Rizzini 1997).
Cortical vascular bundles in the underground stemlike axis of Trixis nobilis (analysed in this study) and Ianthoppapus corymbosus (Melo-de-Pinna and Menezes 2002) confirm the observations from Metcalfe and Chalk (1950) about the occurrence of this kind of vascular tissues in Asteraceae and the tribe Mutisieae.
The anomalous secondary thickening verified in Mikania cordifolia has already been described by Solereder (1908) and Metcalfe and Chalk (1950) for other liana stems of Mikania. It can be considered as another structural trait from aerial systems, which has been conserved in underground organs. Adamson (1934) described the lignified shoots of small shrubs of different genera of Inulaea and the cambium of pericyclic origin, producing phloem and xylem. The author suggested that this kind of anomalous secondary growth should have developed from plants with herbaceous growth form. On the other hand, Mikania sessilifolia, with erect habitus, showed vascular cylinders with secondary phloem, cambium and secondary xylem.
As a conclusion, the formation of aerial shoots from buds located in underground structures associated to the accumulation of fructans reinforces the importance of a viable belowground bud bank for the persistence of forb and subshrub species in grassland physiognomies of the Brazilian Cerrado. It is important to point out the importance of bud-bearing structures in ecosystems under fire influence, such as the rhizomes in tallgrass prairies (Benson et al. 2004), lignotubers in Australia, South Africa and California (Klimesova and Klimes 2007), and the presence of different underground structures (e.g. xylopodia and rhizophores) in the Brazilian Campos grasslands (Fidelis 2008), since they contain the buds and reserve substances needed for vegetation regeneration.
We are grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Process 00/12469-3) for the financial support, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for grants. We also thank Instituto de Botânica and Instituto Florestal in giving permission to collect plant materials, Dr Vinícius C. Souza (USP) for identifying the species and Mrs Marli Kasue Misaki Soares for technical assistance.
ADAMSON RS. 1934. Anomalous secondary thickening in Compositae. Ann Bot 48: 505-514. [ Links ]
ALMEIDA AM ET AL. 2005. Diversidade e ocorrência de Asteraceae em cerrados de São Paulo. Biota Neotropica 5: 1-17. doi: 10.1590/S1676-06032005000300003. [ Links ]
ALONSO AA AND MACHADO SR. 2007. Morphological and developmental investigations of the underground system of Erythroxylum species from Brazilian cerrado. Aust J Bot 55: 749-758. doi: 10.1071/BT070600067-1924/07/070749. [ Links ]
ANDREATA RHP AND MENEZES NL. 1999. Morfoanatomia do embrião, desenvolvimento pós-seminal e origem do rizóforo de Smilax quinquenervia Vell. (Smilacaceae). Bol Bot Univ São Paulo 18: 39-51. [ Links ]
APPEZZATO-DA-GLÓRIA B, CURY G, SOARES MKM, ROCHA R AND HAYASHI AH. 2008A. Underground systems of Asteraceae species from the Brazilian Cerrado. J Torr Bot Soc 135: 103-113. [ Links ]
APPEZZATO-DA-GLÓRIA B, HAYASHI AH, CURY G, SOARES MKM AND ROCHA R. 2008B. Occurrence of secretory structures in underground systems of seven Asteraceae species. Bot J Linn Soc 157: 789-796. [ Links ]
BENSON EJ, HARTNETT DC AND MANN KH. 2004. Belowground bud banks and meristem limitation in tallgrass prairie plant populations. Am J Bot 91: 416-421. [ Links ]
CARVALHO MAM and DIETRICH SMC. 1993. Variation in fructan content in the underground organs of Vernonia herbacea (Vell.) Rusby at different phenological phases. New Phyt 123: 735-740. [ Links ]
COUTINHO LM. 1982. Ecological effects of fire in Brazilian cerrado. In: Huntley BJ and Walker BH (Eds), Ecology of tropical savannas: ecological studies, Berlin: Springer Verlag, p. 273-291. [ Links ]
CURY G AND APPEZZATO-DA-GLÓRIA B. 2009. Internal secretory spaces in thickened underground systems of Asteraceae species. Aust J Bot 57: 229-239. doi: 10.1071/BT08139 0067-1924/09/030229. [ Links ]
DALGLEISH HJ. 2007. Belowground bud banks as regulators of grassland dynamics. Kansas State University, Division of Biology, College of Arts and Sciences, 93 p. [ Links ]
DIAS-TAGLIACOZZO GM, ITAYA NM, CARVALHO MAM, FIGUEIREDO-RIBEIRO RCL AND DIETRICH SMC. 2004. Fructans and water suppression on intact and fragmented rhizophores of Vernonia herbacea. Braz Arch Biol Technol 47: 363-373. doi: 10.1590/S1516-89132004000300005. [ Links ]
FIDELIS A. 2008. Fire in subtropical grasslands in Southern Brazil: effects on plant strategies and vegetation dynamics. Technische Universität München, Fakultat Wissenschaftszentrum Weihenstephan, 150 p. [ Links ]
FIGUEIREDO-RIBEIRO RCL. 1993. Distribuição, aspectos estruturais e funcionais dos frutanos, com ênfase em plantas herbáceas do Cerrado. Rev Bras Fisiol Veg 5: 203-208. [ Links ]
FIGUEIREDO-RIBEIRO RCL, ISEJIMA EM, DIAS-TAGLIACOZZO GM, CARVALHO MAM AND DIETRICH SMC. 1991. The physiological significance of fructan accumulation in Asteraceae from the Cerrado. Cienc Cult 43: 443-446. [ Links ]
FILGUEIRAS TS. 2002. Herbaceous plant communities. In: Oliveira PS and Marquis RJ (Eds), The Cerrados of Brazil: ecology and natural history of a neotropical savanna, Columbia: Columbia University Press, p. 121-139. [ Links ]
HARPER JL. 1977. Population Biology of Plants, New York: Academic Press, 892 p. [ Links ]
HAYASHI AH AND APPEZZATO-DA-GLÓRIA B. 2005. The origin and anatomy of rhizophores in Vernonia herbacea and V. platensis (Asteraceae) from the Brazilian Cerrado. Aust J Bot 53: 273-279. doi: 10.1071/BT04094. [ Links ]
HAYASHI AH AND APPEZZATO-DA-GLÓRIA B. 2007. Anatomy of the underground system in Vernonia grandiflora Less. and V. brevifolia Less. (Asteraceae). Braz Arch Biol Tech 50: 979-988. doi: 10.1590/S1516-89132007000600009. [ Links ]
HENDRY GAF. 1993. Evolutionary origins and natural functions of fructans - a climatological, biogeographic and mechanistic appraisal. New Phyt 123: 3-14. [ Links ]
HOFFMANN WA. 1999. Fire and population dynamics of woody plants in a neotropical savanna: matrix model projections. Ecology 80: 1354-1369. [ Links ]
HUTZLER P, FISCHBACH R, HELLER W, JUNGBLUT TP, REUBER S, SCHMITZ R, VEIT M, WEISSENBO G AND SCHNITZLER JP. 1998. Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J Exp Bot 49: 953-965. [ Links ]
ISEJIMA EM, FIGUEIREDO-RIBEIRO RCL AND ZAIDAN LBP. 1991. Fructan composition in adventitious tuberous roots of Viguiera discolor Baker (Asteraceae) as influenced by daylength. New Phyt 119: 149-154. [ Links ]
ISHARA KL, DÉSTRO GFG, MAIMONI-RODELLA RCS AND YANAGIZAWA Y. 2008. Composição florística de remanescentes de cerrado sensu stricto e Botucatu, SP. Rev Bras Bot 31: 575-586. doi: 10.1590/S0100-84042008000400004. [ Links ]
ITAYA NM, ASEGA AF, CARVALHO MAM AND FIGUEIREDO-RIBEIRO RCL. 2007. Hydrolase and fructosyltransferase activities implicated in the accumulation of different chain size fructans in three Asteraceae species. Plant Phys Bioch 45: 647-656. [ Links ]
JOHANSEN DA. 1940. Plant Microtechnique, New York: McGraw-Hill Book, New York, 523 p. [ Links ]
KATINAS L. 1996. Revision de las especies sudamericanas del genero Trixis (Asteraceae, Mutisieae). Darwiniana 34: 27-108. [ Links ]
KAUFFMAN JB, CUMMINGS DL AND WARD DE. 1994. Relationships of fire, biomass and nutrient dynamics along a vegetation gradient in the Brazilian Cerrado. J Ecol 82: 519-531. [ Links ]
KLIMESOVA J AND KLIMES L. 2007. Bud banks and their role in vegetative regeneration - A literature review and proposal for simple classification and assessment. Persp Plant Ecol Evol Syst 8: 115-129. doi: 10.1016/j.ppees.2006.10.002. [ Links ]
LINDMAN CAM. 1900. Vegetationen i Rio Grande do Sul (Sydbrasilien), Stockholm: Nordin and Josephson, 239 p. [ Links ]
LOTOCKA B AND GESZPRYCH A. 2004. Anatomy of the vegetative organs and secretory structures of Rhaponticum carthamoides (Asteraceae). Bot J Linn Soc 144: 207-233. doi: 10.1111/j.1095-8339.2003.00251.x. [ Links ]
MEDEIROS MB AND MIRANDA HS. 2008. Post-fire resprouting and mortality in cerrado woody plant species over a three-year period. Edinburgh J Bot 65: 53-68. doi: 10.1017/S0960428608004708. [ Links ]
MELO-DE-PINNA GFA AND MENEZES NL. 2002. Vegetative organ anatomy of Ianthopappus corybosus Roque and Hind (Asteraceae-Mutisieae). Rev Bras Bot 25: 505-514. doi: 10.1590/S0100-84042002012000014. [ Links ]
METCALFE CR AND CHALK L. 1950. Anatomy of the Dicotyledons: leaves, stem and wood in relation to taxonomy with notes on economic uses, Oxford: Clarendon Press, 1500 p. [ Links ]
ELSON J AND SPOLLEN WG. 1987. Fructans. Physiol Plant 71: 512-516. [ Links ]
ORTHEN B. 2001. Sprouting of the fructan - and starch-storing geophyte Lachenalia minima: effects on carbohydrate and water content within the bulbs. Phisiol Plant 113: 308-314. doi: 10.1111/j.1399-3054.2001.1130302.x. [ Links ]
PAVIANI TI. 1987. Anatomia do desenvolvimento do xilopódio de Brasilia sickii G.M. Barroso. Estágio inicial. Cienc Cult 39: 399-405. [ Links ]
PONTIS HG. 1989. Fructans and cold stress. J Plant Phys 134: 148-150. [ Links ]
PORTES MT AND CARVALHO MAM. 2006. Spatial distribution of fructan and fructan metabolizing enzymes in rhizophores of Vernonia herbacea (Vell.) Rusby (Asteraceae) in different developmental phases. Plant Sci 170: 624-633. doi: 10.1016/j.plantsci.2005.10.017. [ Links ]
RIZZINI CT. 1965. Estudos experimentais sobre o xilopódio e outros órgãos tuberosos de plantas do Cerrado. An Acad Bras Cienc 37: 87-113. [ Links ]
RIZZINI CT. 1997. Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos, Rio de Janeiro: Âmbito Cultural Edições Ltda, 747 p. [ Links ]
RIZZINI CT AND HERINGER EP. 1961. Underground organs of plants from some southern brazilian savannas, with special reference to the xylopodium. Phyton 17: 105-124. [ Links ]
SAKAI WS. 1973. Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Technol 48: 247-249. [ Links ]
SOARES JJ, SOUZA MHA AND LIMA MI. 2006. Twenty years of post-fire plant succession in a "cerrado", São Carlos, SP, Brazil. Braz J Biol 66(2B): 587-602. doi: 10.1590/S1519-69842006000400003. [ Links ]
SOLEREDER H. 1908. Systematic anatomy of Dicotyledons, Oxford: Clarendon Press. [ Links ]
TALBOTT LD AND ZEIGER E. 1998. The role of sucrose in guard cell osmoregulation. J Exp Bot 49: 329-337. [ Links ]
TERTULIANO MF AND FIGUEIREDO-RIBEIRO RCL. 1993. Distribution of fructose polymers in herbaceous species of Asteraceae from the cerrado. New Phyt 123: 741-749. [ Links ]
VERDAGUER D AND OJEDA F. 2005. Evolutionary transition from resprouter to seeder life history in two Erica (Ericaceae) species: insights from seedling axillary buds. Ann Bot 95: 593-599. [ Links ]
VILHALVA DAA AND APPEZZATO-DA-GLÓRIA B. 2006. Morfo-anatomia do sistema subterrâneo de Calea verticillata (Klatt) Pruski e Isostigma megapotamicum (Spreng.) Sherff-Asteraceae. Rev Bras Bot 29: 39-17. doi: 10.1590/S0100-84042006000100005. [ Links ]
Manuscript received on June 8, 2010; accepted for publication on August 24, 2010