Unveiling the hidden reserves: allocation strategies associated with underground organs of Cerrado legumes in fire-prone savannas
Bruno Bonadio Cozin A , Tassia Caroline Ferreira A , L. Felipe Daibes B , Isabella Fiorini de Carvalho A , Beatriz Silvério dos Santos A , Roberta Possas de Souza A , Liliane Santos de Camargos A and Aline Redondo Martins A *A
B
Abstract
The synthesis and differential allocation of reserve compounds is an important adaptive mechanism that enables species to resprout in fire-prone ecosystems. The analysis of compound allocation dynamics (differential accumulation of compounds between plant organs) provides insights into plant responses to disturbances. The aim was to quantify reserves in eight legume species from Cerrado open savannas with high fire frequency in order to investigate the patterns of allocation and distribution of compounds between leaves and underground organs, drawing ecophysiological inferences. The species were collected in ‘campo sujo’ areas of the Cerrado. Leaves and underground organs (xylopodium, taproot tubers) were subjected to physiological analyses. Overall, underground organs were characterised by greater deposits of carbohydrates, mainly soluble sugars, and also with the accumulation of proteins and amino acids. This suggests that nitrogen reserves, as well as carbohydrates, may have an ecophysiological function in response to fire, being allocated to the underground organs. Phenols were mainly evident in leaves, but a morphophysiological pattern was identified, where the two species with taproot tubers tended to concentrate more phenols in the underground portion compared to species with xylopodium, possibly due to functional differences between these organs. Such data allow inferring relevant ecophysiological dynamics in legumes from open savannas.
Keywords: allocation, carbon compounds, Cerrado, ecophysiology, leaves, nitrogen compounds, taproot tuber, xylopodium.
References
Almeida VO, Carneiro RV, Carvalho MAM, Figueiredo-Ribeiro RCL, Moraes MG (2015) Diversity of non-structural carbohydrates in the underground organs of five Iridaceae species from the Cerrado (Brazil). South African Journal of Botany 96, 105-111.
| Crossref | Google Scholar |
Appezzato-da-Glória B, Cury G (2011) Morpho-anatomical features of underground systems in six Asteraceae species from the Brazilian Cerrado. Anais da Academia Brasileira de Ciências 83, 981-992.
| Crossref | Google Scholar |
Appezzato-da-Glória B, Estelita MEM (2000) The developmental anatomy of the subterranean system in Mandevilla illustris (Vell.) Woodson and M. velutina (Mart. ex Stadelm.) Woodson (Apocynaceae). Revista Brasileira de Botânica 23, 27-35.
| Crossref | Google Scholar |
Appezzato-da-Glória B, Cury G, Kasue Misaki Soares M, Rocha R, Hissae Hayashi A (2008) Underground systems of Asteraceae species from the Brazilian Cerrado. The Journal of the Torrey Botanical Society 135, 103-113.
| Crossref | Google Scholar |
Augustine DJ, Derner JD, Milchunas DG (2010) Prescribed fire, grazing, and herbaceous plant production in shortgrass steppe. Rangeland Ecology & Management 63, 317-323.
| Crossref | Google Scholar |
Azani N, Babineau M, Bailey CD, Banks H, Barbosa AR, Pinto RB, Boatwright JS, Borges LM, Brown GK, Bruneau A, Candido E, Cardoso D, Chung K-F, Clark RP, Conceição AdS, Crisp M, Cubas P, Delgado-Salinas A, Dexter KG, Doyle JJ, Duminil J, Egan AN, de la Estrella M, Falcão MJ, Filatov DA, Fortuna-Perez AP, Fortunato RH, Gagnon E, Gasson P, Rando JG, de Azevedo Tozzi AMG, Gunn B, Harris D, Haston E, Hawkins JA, Herendeen PS, Hughes CE, Iganci JRV, Javadi F, Kanu SA, Kazempour-Osaloo S, Kite GC, Klitgaard BB, Kochanovski FJ, Koenen EJM, Kovar L, Lavin M, le Roux M, Lewis GP, de Lima HC, López-Roberts MC, Mackinder B, Maia VH, Malécot V, Mansano VF, Marazzi B, Mattapha S, Miller JT, Mitsuyuki C, Moura T, Murphy DJ, Nageswara-Rao M, Nevado B, Neves D, Ojeda DI, Pennington RT, Prado DE, Prenner G, de Queiroz LP, Ramos G, Filardi FLR, Ribeiro PG, de Lourdes Rico-Arce M, Sanderson MJ, Santos-Silva J, São-Mateus WMB, Silva MJS, Simon MF, Sinou C, Snak C, de Souza ÉR, Sprent J, Steele KP, Steier JE, Steeves R, Stirton CH, Tagane S, Torke BM, Toyama H, da Cruz DT, Vatanparast M, Wieringa JJ, Wink M, Wojciechowski MF, Yahara T, Yi T, Zimmerman E (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: The Legume Phylogeny Working Group (LPWG). TAXON 66, 44-77.
| Crossref | Google Scholar |
Batalha MA, Silva IA, Cianciaruso MV, de Carvalho GH (2011) Trait diversity on the phylogeny of cerrado woody species. Oikos 120, 1741-1751.
| Crossref | Google Scholar |
Beerling DJ, Osborne CP (2006) The origin of the savanna biome. Global Change Biology 12, 2023-2031.
| Crossref | Google Scholar |
Bell TL, Pate JS, Dixon KW (1996) Relationships between fire response, morphology, root anatomy and starch distribution in south-west Australian Epacridaceae. Annals of Botany 77, 357-364.
| Crossref | Google Scholar |
Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Analytical Biochemistry 17, 278-293.
| Crossref | Google Scholar | PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
| Crossref | Google Scholar | PubMed |
Bruneau A, Doyle JJ, Herendeen P, Hughes C, Kenicer G, Lewis G, Mackinder B, Pennington RT, Sanderson MJ, Wojciechowski MF, Boatwright S, Brown G, Cardoso D, Crisp M, Egan A, Fortunato RH, Hawkins J, Kajita T, Klitgaard B, Koenen E, Lavin M, Luckow M, Marazzi B, McMahon MM, Miller JT, Murphy DJ, Ohashi H, de Queiroz LP, Rico L, Särkinen T, Schrire B, Simon MF, Souza ER, Steele K, Torke BM, Wieringa JJ, van Wyk B-E (2013) Legume phylogeny and classification in the 21st century: progress, prospects and lessons for other species–rich clades. TAXON 62, 217-248.
| Crossref | Google Scholar |
Campos GR, Carneiro RGdS, Ferreira HD, Bortolini JC, Moraes MGd (2021) Non-structural carbohydrates stored in belowground organs point to the diversity in Amaranthaceae. Flora 276–277, 151774.
| Crossref | Google Scholar |
Charles-Dominique T, Beckett H, Midgley GF, Bond WJ (2015) Bud protection: a key trait for species sorting in a forest–savanna mosaic. New Phytologist 207, 1052-1060.
| Crossref | Google Scholar | PubMed |
Clarke PJ, Lawes MJ, Midgley JJ, Lamont BB, Ojeda F, Burrows GE, Enright NJ, Knox KJE (2013) Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytologist 197, 19-35.
| Crossref | Google Scholar | PubMed |
Clarke PJ, Manea A, Leishman MR (2016) Are fire resprouters more carbon limited than non-resprouters? Effects of elevated CO2 on biomass, storage and allocation of woody species. Plant Ecology 217, 763-771.
| Crossref | Google Scholar |
Corbesier L, Havelange A, Lejeune P, Bernier G, Périlleux C (2001) N content of phloem and xylem exudates during the transition to flowering in Sinapis alba and Arabidopsis thaliana. Plant, Cell & Environment 24, 367-375.
| Crossref | Google Scholar |
Coutinho LM (1978) O conceito de cerrado. Revista Brasileira de Botânica 1, 17-23.
| Google Scholar |
Coutinho LM (1990) Fire in the Ecology of the Brazilian Cerrado. In ‘Fire in the tropical biota’. (Ed. JG Goldammer) pp. 82–105. (Springer) https://doi.org/10.1007/978-3-642-75395-4_6
Daldegan G, De Carvalho O, Guimarães R, Gomes R, Ribeiro F, McManus C (2014) Spatial patterns of fire recurrence using remote sensing and GIS in the Brazilian Savanna: Serra do Tombador Nature Reserve, Brazil. Remote Sensing 6, 9873-9894.
| Crossref | Google Scholar |
de Moraes MG, de Carvalho MAM, Franco AC, Pollock CJ, Figueiredo-Ribeiro RdCL (2016) Fire and drought: soluble carbohydrate storage and survival mechanisms in herbaceous plants from the Cerrado. BioScience 66, 107-117.
| Crossref | Google Scholar |
de Oliveira Joaquim E, Moura Silva T, Leone Figueiredo-Ribeiro RdC, Gomes de Moraes M, Machado de Carvalho MA (2018) Diversity of reserve carbohydrates in herbaceous species from Brazilian campo rupestre reveals similar functional traits to endure environmental stresses. Flora 238, 201-209.
| Crossref | Google Scholar |
Dinkeloo K, Boyd S, Pilot G (2018) Update on amino acid transporter functions and on possible amino acid sensing mechanisms in plants. Seminars in Cell & Developmental Biology 74, 105-113.
| Crossref | Google Scholar | PubMed |
El Omari B, Aranda X, Verdaguer D, Pascual G, Fleck I (2003) Resource remobilization in Quercus ilex L. resprouts. Plant and Soil 252, 349-357.
| Crossref | Google Scholar |
Ferraro A, da Silva GS, de Aguiar CL, Appezzato-da-Glória B (2021) Evaluating belowground bud banks of native species from Cerrado: structural, chemical, and ecological approaches. Flora 281, 151852.
| Crossref | Google Scholar |
Fidelis A, Zirondi HL (2021) And after fire, the Cerrado flowers: a review of post-fire flowering in a tropical savanna. Flora 280, 151849.
| Crossref | Google Scholar |
Folin O, Ciocalteu V (1927) On tyrosine and tryptophane determinations in proteins. Journal of Biological Chemistry 73, 627-650.
| Crossref | Google Scholar |
Foreman D, Gaylor L, Evans E, Trella C (1973) A modification of the Roe procedure for determination of fructose in tissues with increased specificity. Analytical Biochemistry 56, 584-590.
| Crossref | Google Scholar | PubMed |
Franco AC, Rossatto DR, de Carvalho Ramos Silva L, da Silva Ferreira C (2014) Cerrado vegetation and global change: the role of functional types, resource availability and disturbance in regulating plant community responses to rising CO2 levels and climate warming. Theoretical and Experimental Plant Physiology 26, 19-38.
| Crossref | Google Scholar |
Fundação Grupo Boticário (2011) Plano de Manejo da Reserva Natural da Serra do Tombador, Cavalcante – Goiás. (Fundação Grupo Boticário: Curitiba). Available at https://www.fundacaogrupoboticario.org.br/pt/Biblioteca/pmt_plano_manejo_TOMBADOR.pdf [Accessed 21 December 2023]
Geiger DR, Servaites JC, Fuchs MA (2000) Role of starch in carbon translocation and partitioning at the plant level. Functional Plant Biology 27, 571.
| Crossref | Google Scholar |
Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. The Plant Journal 39, 847-862.
| Crossref | Google Scholar | PubMed |
Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know. New Phytologist 211, 386-403.
| Crossref | Google Scholar | PubMed |
Hayashi AH, Appezzato-da-Glória B (2007) Anatomy of the underground system in Vernonia grandiflora Less. and V. brevifolia Less. (Asteraceae). Brazilian Archives of Biology and Technology 50, 979-988.
| Crossref | Google Scholar |
Hutzler P, Fischbach R, Heller W, Jungblut TP, Reuber S, Schmitz R, Veit M, Weissenbock G, Schnitzler J-P (1998) Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. Journal of Experimental Botany 49, 953-965.
| Crossref | Google Scholar |
Janeček Š, Bartušková A, Bartoš M, Altman J, de Bello F, Doležal J, Latzel V, Lanta V, Lepš J, Klimešová J (2015) Effects of disturbance regime on carbohydrate reserves in meadow plants. AoB Plants 7, plv123.
| Crossref | Google Scholar |
Joaquim EO, Hayashi AH, Torres LMB, Figueiredo-Ribeiro RCL, Shiomi N, de Sousa FS, Lago JHG, Carvalho MAM (2018) Chemical structure and localization of levan, the predominant fructan type in underground systems of Gomphrena marginata (Amaranthaceae). Frontiers in Plant Science 9, 1745.
| Crossref | Google Scholar |
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. Journal of Statistical Software 25, 1-18.
| Crossref | Google Scholar |
Marques AR, Garcia QS, Rezende JLP, Fernandes GW (2000) Variations in leaf characteristics of two species of Miconia in the Brazilian cerrado under different light intensities. Tropical Ecology 41, 47-60.
| Google Scholar |
Miyanishi K, Kellman M (1986) The role of root nutrient reserves in regrowth of two savanna shrubs. Canadian Journal of Botany 64, 1244-1248.
| Crossref | Google Scholar |
Moraes MG, Chatterton NJ, Harrison PA, Filgueiras TS, Figueiredo-Ribeiro RCL (2013) Diversity of non-structural carbohydrates in grasses (Poaceae) from Brazil. Grass and Forage Science 68, 165-177.
| Crossref | Google Scholar |
Palacio S, Maestro M, Montserrat-Martí G (2007) Relationship between shoot-rooting and root-sprouting abilities and the carbohydrate and nitrogen reserves of Mediterranean dwarf shrubs. Annals of Botany 100, 865-874.
| Crossref | Google Scholar | PubMed |
Pate JS, Froend RH, Bowen BJ, Hansen A, Kuo J (1990) Seedling growth and storage characteristics of seeder and resprouter species of mediterranean-type ecosystems of S. W. Australia. Annals of Botany 65, 585-601.
| Crossref | Google Scholar |
Pausas JG, Lamont BB, Paula S, Appezzato-da-Glória B, Fidelis A (2018) Unearthing belowground bud banks in fire-prone ecosystems. New Phytologist 217, 1435-1448.
| Crossref | Google Scholar | PubMed |
Pilon NAL, Cava MGB, Hoffmann WA, Abreu RCR, Fidelis A, Durigan G (2021) The diversity of post-fire regeneration strategies in the cerrado ground layer. Journal of Ecology 109, 154-166.
| Crossref | Google Scholar |
Pivello VR, Oliveras I, Miranda HS, Haridasan M, Sato MN, Meirelles ST (2010) Effect of fires on soil nutrient availability in an open savanna in Central Brazil. Plant and Soil 337, 111-123.
| Crossref | Google Scholar |
Pollock CJ (1986) Tansley review no. 5 fructans and the metabolism of sucrose in vascular plants. New Phytologist 104, 1-24.
| Crossref | Google Scholar | PubMed |
Rasheed F, Markgren J, Hedenqvist M, Johansson E (2020) Modeling to understand plant protein structure-function relationships—implications for seed storage proteins. Molecules 25, 873.
| Crossref | Google Scholar | PubMed |
R Core Team (2023) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing) Available at https://www.R-project.org/
Rizzini CT, Heringer EP (1961) Underground organs of plants from some southern Brazilian savannas, with special reference to the xylopodium. Phyton 17, 105-124.
| Google Scholar |
Rodrigues CA, Fidelis A (2022) Should we burn the Cerrado? Effects of fire frequency on open savanna plant communities. Journal of Vegetation Science 33, 13159.
| Crossref | Google Scholar |
Rosalem PF, Martins AR, Camargos LS (2022) How can the analysis of reserve dynamics after fire support the phenological insight of Bulbostylis paradoxa (Spreng.) Lindm (Cyperaceae)? Plant Physiology and Biochemistry 182, 167-173.
| Crossref | Google Scholar | PubMed |
Rossatto DR, Kolb RM (2010) Gochnatia polymorpha (Less.) Cabrera (Asteraceae) changes in leaf structure due to differences in light and edaphic conditions. Acta Botanica Brasilica 24, 605-612.
| Crossref | Google Scholar |
Silva GSd, Ferraro A, Ogando FIB, Aguiar CLd, Appezzato-da-Glória B (2020) Structures related to resprouting potential of two Myrtaceae species from Cerrado: morpho-anatomical and chemical studies. Anais da Academia Brasileira de Ciências 92, e20180472.
| Crossref | Google Scholar |
Simon MF, Pennington T (2012) Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado. International Journal of Plant Sciences 173, 711-723.
| Crossref | Google Scholar |
Simon MF, Grether R, de Queiroz LP, Skema C, Pennington RT, Hughes CE (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of Sciences 106, 20359-20364.
| Crossref | Google Scholar |
Souza A, Sandrin CZ, Calió MFA, Meirelles ST, Pivello VR, Figueiredo-Ribeiro RCL (2010) Seasonal variation of soluble carbohydrates and starch in Echinolaena inflexa, a native grass species from the Brazilian savanna, and in the invasive grass Melinis minutiflora. Brazilian Journal of Biology 70, 395-404.
| Crossref | Google Scholar |
Tertuliano MF, Figueiredo-Ribeiro RCL (1993) Distribution of fructose polymers in herbaceous species of Asteraceae from the cerrado. New Phytologist 123, 741-749.
| Crossref | Google Scholar |
Trovato M, Funck D, Forlani G, Okumoto S, Amir R (2021) Editorial: Amino acids in plants: regulation and functions in development and stress defense. Frontiers in Plant Science 12, 772810.
| Crossref | Google Scholar |
Umbreit WW, Kingsley GR, Schaffert RR, Siplet H (1957) A colorimetric method for transaminase in serum or plasma. The Journal of Laboratory and Clinical Medicine 49, 454-459.
| Google Scholar | PubMed |
van Handel E (1968) Direct microdetermination of sucrose. Analytical Biochemistry 22, 280-283.
| Crossref | Google Scholar | PubMed |
Vieira EA, Silva MdG, Moro CF, Laura VA (2017) Physiological and biochemical changes attenuate the effects of drought on the Cerrado species Vatairea macrocarpa (Benth.) Ducke. Plant Physiology and Biochemistry 115, 472-483.
| Crossref | Google Scholar | PubMed |
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochemical Journal 57, 508-514.
| Crossref | Google Scholar | PubMed |
Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. The Analyst 80, 209.
| Crossref | Google Scholar |
Zupo T, Daibes LF, Pausas JG, Fidelis A (2021) Post-fire regeneration strategies in a frequently burned Cerrado community. Journal of Vegetation Science 32, e12968.
| Crossref | Google Scholar |