Abstract
Allelopathy has been considered a key mechanism to explain the invasiveness of some species. It is well known that invasive plants can affect native plants by producing novel allelochemicals but some exotic plant species may be also sensitive to allelochemicals released by native species, providing a tool to reduce growth and impacts of invasive exotic species. Here, using growth chamber experiments we tested the mutual potential allelopathic effects of Sesbania virgata (a native dominant species) and the alien Leucaena leucocephala seeds. S. virgata was unaffected by seed leachates of L. leucocephala, indicating that, under lab conditions, this legume presents resistance to the phytotoxic compounds produced by seeds of this alien species. In contrast, germination and seedling growth of L. leucocephala were strongly affected by the phytochemicals produced by seeds of S. virgata. A delay in endospermic mobilization of storage carbohydrates (raffinose-family oligosaccharides and galactomannan) was observed in the alien species. These potential allelopathic effects could not be attributed sole to the presence neither of the phytoxic catechin nor of ABA in seed leachates of S. virgata. Our findings indicate that the in vitro behavior of S. virgata is consistent with its aggressiveness in natural environment and suggest sesbanimide as a potential candidate as implicated in the noxious effects of S. virgata on the alien species.
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References
Amaral LIV, Costa PMF, Aidar APM, Gaspar M, Buckeridge MS (2007) A new rapid and sensitive enzymatic method for extraction and quantification of starch in plant material. Hoehnea 34:425–431. doi:10.1590/S2236-89062007000400001
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development germination and dormancy, 3rd edn. Springer, New York, pp 203–208. doi:10.1007/978-1-4614-4693-4
Blair AC, Hanson BD, Brunk GR, Marrs RA, Westra P, Nissen SJ, Hufbauer RA (2005) New techniques and findings in the study of a candidate allelochemical implicated in invasion success. Ecol Lett 10:1039–1047. doi:10.1111/j.1461-0248.2005.00805.x
Blair AC, Nissen SJ, Brunk GR, Hufbauer RA (2006) A lack of evidence for an ecological role of the putative allelochemical (±)-catechin in spotted knapweed invasion success. J Chem Ecol 32:2327–2331. doi:10.1007/s10886-006-9168-y
Blair AC, Weston LA, Nissen SJ, Brunk GR, Hufbauer RA (2009) The importance of analytical techniques in allelopathy studies with the reported allelochemical catechin as an example. Biol Invasions 11:325–332. doi:10.1007/s10530-008-9250-1
Bongard C (2012) A review of the influence of root-associating fungi and root exudates on the success of invasive plants. NeoBiota 14:21–45. doi:10.3897/neobiota.14.2927
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantitis of protein utilizing the principle of protein-dye binding. Ann Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Buckeridge MS, Dietrich SMC (1990) Galactomannan from Brazilian legume seeds. Rev Bras Bot 13:109–112
Buckeridge MS, Dietrich SMC (1996) Mobilisation of the raffinose family oligosacharides and galactomannan in germinating seeds of Sesbania marginata Benth. (Leguminosae-Faboideae). Plant Sci 117:33–43. doi:10.1016/0168-9452(96)04410-x
Buckeridge MS, Dietrich SMC, De Lima DU (2000) Galactomannans as the reserve carbohydrate in legume seeds. Carbohydrate reserves in plants-synthesis and regulation. Develop Crop Sci 26:283–316. doi:10.1016/0168-9452(96)04410-x
Caccere R, Teixeira SP, Centeno DC, Figueiredo-Ribeiro RCL, Braga MR (2013) Metabolic and structural changes during early maturation of Inga vera seeds are consistent with the lack of a desiccation phase. J Plant Physiol 170:791–800. doi:10.1016/j.jplph.2013.01.002
Callaway RM, Aschehoug (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523. doi:10.1126/science.290.5491.521
Callaway RM, Ridenour WM (2004) Novel weapons: a biochemically-based hypothesis for invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443. doi:10.1890/1540-9295(2004)002[0436:NWISAT]2.0.CO;2
Carvalho CP, Hayashi AH, Braga MR, Nievola CC (2013) Biochemical and anatomical responses related to the in vitro survival of the tropical bromeliad Nidularium minutum to low temperatures. Plant Physiol Bioch 71:144–154. doi:10.1016/j.plaphy.2013.07.005
Ceballos L, Hossaert-Mckey M, Mckey D, Andary C (1998) Rapid deployment of allelochemicals in exudates of germinating seeds of Sesbania (Fabaceae): roles of seed anatomy and histolocalization of polyphenolic compounds in anti-pathogen defense of seedlings. Chemoecology 8:141–151. doi:10.1007/s000490050019
Chobot V, Huber C, Trettenhahn G, Hadacek F (2009) (+/−)-catechin: chemical weapon, antioxidant, or stress regulator? J Chem Ecol 35:980–996. doi:10.1007/s10886-009-9681-x
Christina M, Rouifed S, Puijalon S, Vallier F, Meiffren G, Bellvert F, Piola F (2015) Allelopathic effect of a native species on a major plant invader in Europe. Sci Nat 102:1. doi:10.1007/s00114-015-1263-x
Coelho LCS (2014) Potencial alelopático in vitro dos exsudatos de Sesbania virgata (cav.) pers. sobre tomate e arroz e em fungos micorrízicos arbusculares na fase assimbiótica. Ph.D. thesis State University of Campinas
Coutinho MP, Carneiro JGA, Barroso DG, Rodrigues LA, Figueiredo FAMMA, Mendonça AVR, Novaes AB (2005) Growth of seedlings of Sesbania virgata (Cav.) Pers. planted on degraded area by clay extraction. Floresta 35:231–239. doi:10.5380/rf.v35i2.4608
Crounse RJ, Maxwell JD, Blank H (1962) Inhibition of growth of hair by mimosine. Nature 194:194–195. doi:10.1038/194694b0
Cummings JA, Parker IM, Gilbert GS (2012) Allelopathy: a tool for weed management in forest restoration. Plant Ecol 213:1975–1989. doi:10.1007/s11258-012-0154-x
De Souza VC, Agra PFM, Andrade LA, Oliveira IG, De Oliveira LS (2010) Germination of seeds of the invasive plant Sesbania virgata (Cav.) Pers. under effects of light, temperature, and dormancy overcoming. Ciências Agrárias 31:889–894. doi:10.5433/1679-0359.2010v31n4p889
Del Fabbro C, Gusewell S, Prati D (2014) Allelopathic effects of three plant invaders on germination of native species: a field study. Biol Invasions 16:1035–1042. doi:10.1007/s10530-013-0555-3
Dirk LMA, Van der Krol AR, Vreugdenhil D, Hilhorst HWM, Bewley JD (1999) Galactomannan, soluble sugar and starch mobilization following germination of Trigonella foenum-graecum seeds. Plant Physiol Biochem 37:41–50. doi:10.1016/S0981-9428(99)80065-5
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. doi:10.1021/ac60111a017
El Id VL, Da Costa BV, Mignoni DSB, Veronesi MB, Simoões K, Braga MR, Dos Santos NA Jr (2015) Phytotoxic effect of Sesbania virgata (Cav.) Pers. on seeds of agronomic and forestry species. J For Res 26:339–346. doi:10.1007/s11676-015-0026-z
Feria MJ, Lopez ZF, Garcia JC, Perez A, Zamudio MAM, Alfaro A (2011) Valorization of Leucaena leucocephala for energy and chemicals from auto-hydrolysis. Biomass Bioenerg 35:2224–2233. doi:10.1016/j.biombioe.2011.02.038
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Cienc Agrotec 35:1039–1042. doi:10.1590/S1413-70542011000600001
Fitter A (2003) Ecology. Making allelopathy respectable. Science 301:1337–1338. doi:10.1126/science.1089291
GISP Programme Contribution to the Global Invasive Species (2004) Tropical Asia Invaded: The growing danger of invasive alien species. The Global Invasive Species Programme pp. 80
Gomes M, Garcia Q (2013) Reactive oxygen species and seed germination. Biologia 68:351–357. doi:10.2478/s11756-013-0161-y
Gorst-Allman CP, Steyn PS, Vleggaar R, Grobbelaar N (1984) Structure elucidation of sesbanimide using high field RMN spectroscopy. J Chem Soc 1:1311–1314. doi:10.1039/P19840001311
Harun MAYA, Robinson RW, Johnson J, Uddin MN (2014) Allelopathic potential of Chrysanthemoides monilifera subsp. monilifera (boneseed): a novel weapon in the invasion processes. S Afr J Bot 93:157–166. doi:10.1016/j.sajb.2014.04.008
He W-M, Feng Y, Ridenour WM, Thelen GC, Pollock JL, Diaconu A, Callaway RM (2009) Novel weapons and invasions: biogeographic differences in the competitive effects of Centaurea maculosa and its root exudates (+)-catechin. Oecologia 159:803–815. doi:10.1007/s00442-008-1234-4
Hierro J, Callaway R (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39. doi:10.1023/A:1026208327014
Hoffmann JH, Moran VC (1998) The population dynamics of an introduced tree, Sesbania punicea, in South Africa, in response to long-term damage caused by different combinations of three species of biological control agents. Oecologia 114:343–348. doi:10.1007/s004420050456
Inderjit, Duke SO (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539. doi:10.1007/s00425-003-1054-z
Inderjit, Wardle DA, Karban R, Callaway RM (2011) The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol 26:655–662. doi:10.1016/j.tree.2011.08.003
Jefferson LV, Pennacchio M (2003) Allelopathic effects of foliage extracts from four Chenopodiaceae species on seed germination. J Arid Environ 55:275–285. doi:10.1016/S0140-1963(03)00028-4
Kim YOK, Lee EJ (2011) Comparison of phenolic compounds and the effects of invasive and native species in East Asia: support for the novel weapons hypothesis. Ecol Res 26:87–94. doi:10.1007/s11284-010-0762-7
Kissmann KG, Groth D (1999) Infesting and noxious plants, 1st edn. Brazilian BASF, São Paulo, pp 770–776
Lara-Núñez A, Sánchez-Nieto S, Anaya AL, Cruz Ortega R (2009) Phytotoxic effects of Sicyos deppei (Cucurbitaceae) in germinating tomato seeds. Physiol Plant 136:180–192. doi:10.1111/j.1399-3054.2009.01228.x
Leduc SNM, Silva JPN, Gaspar M, Barbedo CJ, Figueiredo-Ribeiro RCL (2012) Non-structural carbohydrates of immature seeds of Caesalpinia echinata (Leguminosae) are involved in the induction of desiccation tolerance. Aust J Bot 60:42–48. doi:10.1071/BT11236
Lind E, Parker JD (2010) Novel weapons testing: are invasive plants more chemically defended than native plants? PLoS ONE 5:e10429. doi:10.1371/journal.pone.0010429
Loydi A, Donath TW, Eckstein RL, Otte A (2015) Non-native species litter reduces germination and growth of resident forbs and grasses: allelopathic, osmotic or mechanical effects? Biol Invasions 17:581–595. doi:10.1007/s10530-014-0750-x
Maguire JD (1962) Speed of germination-aid in selection and evaluation for seedling. Emerg Vigor Crop Sci 2:176–177. doi:10.2135/cropsci1962.0011183X0002000020033x
Marques AR, Costa CF, Atman APF, Garcia QS (2014) Germination characteristics and seedbank of the alien species Leucaena leucocephala (Fabaceae) in Brazilian forest: ecological implications. Weed Res 54:576–583. doi:10.1111/wre.12107
McCleary BV (1983) Enzymic interaction in the hydrolysis of galactomannan in germinating guar: the role of exo-β-mannanase. Phytochemistry 22:649–658. doi:10.1016/S0031-9422(00)86956-3
Mello JIO, Barbedo CJ, Salatino A, Figueiredo-Ribeiro RCL (2010) Reserve carbohydrates and lipids from the seeds of four tropical tree species with different sensitivity to desiccation. Braz Arch Biol Techn 53:889–899. doi:10.1590/S1516-49789132010000400019
Nickerson K, Flory SL (2015) Competitive and allelopathic effects of the invasive shrub Schinus terebinthifolius (Brazilian peppertree). Biol Invasions 17:555–564. doi:10.1007/s10530-014-0748-4
Nóbrega RSA, De Paula AM, Boas AMV, Nóbrega CZ, Moreira FMS (2008) Morphological parameters of Sesbania virgata (Cav.) Pers and Anadenanthera peregrina (L.) seedlings cultivated in substrate fertilized with urban waste compost. Rev Arvore 32:597–607. doi:10.1590/S0100-67622008000300020
Pierik R, Mommer L, Voesenek LACJ (2013) Molecular mechanisms of plant competition: neighbor detection and response strategies. Funct Ecol 27:841–853. doi:10.1111/1365-2435.12010
Popovici J, Bertrand C, Jacquemoud D, Bellvert F, Fernandez MP, Comte G, Piola F (2011) An allelochemical from Myrica gale with strong phytotoxic activity against highly invasive Fallopia x bohemica taxa. Molecules 16:2323–2333. doi:10.3390/molecules16032323
Potomati A, Buckeridge MS (2002) Effect of abscisic acid on the mobilisation of galactomannan and embryo development of Sesbania virgata (Cav.) Pers. (Leguminosae-Faboideae). Rev Bras Bot 25:303–310. doi:10.1590/S0100-51284042002000300006
Pott A, Pott VJ (1994) Plants of Pantanal. Center for Agricultural Research in the Pantanal, Corumbá, p 320
Powell RG, Plattner RD, Suffness M (1990) Ocurrence of sesbanimide in seeds of toxic Sesbania species. Weed Sci 38:148–152
Praxedes PG, Zerlin JK, Dias LO, Pessoni RAB (2011) A novel antifungal protein from seeds of Sesbania virgata (Cav.) Pers. (Leguminosae-Faboideae). Braz J Biol 71:687–692. doi:10.1590/S1519-69842011000400013
Reid JSG, Meier H (1973) Enzymic activities and galactomannan mobilisation in germinating seeds of fenugreek (Trigonella foenum-graecum L. Leguminosae). Secretion of α-galactosidase and β-mannosidase by the aleurone layer. Planta 112:301–308. doi:10.1007/BF00390303
Schaffner U, Ridenour WM, Wolf VC, Bassett T, Muller C, Muller-scharer H, Sutherland S, Lortie CJ, Callaway RM (2011) Plant invasions, generalist herbivores, and novel defense weapons. Ecology 92:829–835. doi:10.1890/10-1230.1
Simões K, Du J, Kretzschmar FS, Broeckling CD, Stermitz F, Vivanco JM, Braga MR (2008) Phytotoxic catechin leached by seeds of the tropical weed Sesbania virgata. J Chem Ecol 34:681–687. doi:10.1007/s10886-008-9443-1
Singh HP, Batish DR, Pandher JK, Kohli RK (2003) Assessment of allelopathic properties of Parthenium hysterophorus residues. Agr Ecosyst Environ 95:537–541. doi:10.1016/S0167-8809(02)00202-5
Souza VC, Andrade LA, Bezerra FTC, Fabricante JR, Feitosa RC (2011) Evaluation population of Sesbania virgata (Cav.) Pers. (Fabaceae Lindl.), on the banks of Paraíba river. Braz J Agric Sci 6:314–320. doi:10.5039/agraria.v6i2a926
Teasdale JR, Rice CP, Cai G, Mangum RW (2012) Expression of allelopathy in the soil environment: soil concentration and activity of benzoxazinoid compounds released by rye cover crop residue. Plant Ecol 213:1893–1905. doi:10.1007/s11258-012-0057-x
Thorpe AS, Thelen GC, Diaconu A, Callaway RM (2009) Root exudate is allelopathic in invaded community but not in native community: field evidence for the novel weapons hypothesis. J Ecol 97:641–645. doi:10.1111/j.1365-2745.2009.01520.x
Tonini PP, Lisboa CGS, Freschi L, Mercier H, Mazzoni-Viveiros SC, Buckeridge MS (2006) Effect of abscisic acid on galactomannan degradation and endo-β-mannanase activity in seeds of Sesbania virgata (Cav.) Pers. (Leguminosae). Trees Struct Funct 20:669–678. doi:10.1007/s00468-006-0082-2
Tonini PP, Lisboa CGS, Silva CO, Mazzoni-Viveiros SC, Buckeridge MS (2007) Testa is involved in the control of storage mobilisation in seeds of Sesbania virgata (Cav.) Pers. a tropical legume tree from of the Atlantic Forest. Trees 21:13–21. doi:10.1007/s00468-006-0091-1
Tonini PP, Purgatto E, Buckeridge MS (2010) Effects of abscisic acid, ethylene and sugars on the mobilization of storage proteins and carbohydrates in seeds of the tropical tree Sesbania virgata (Leguminosae). Ann Bot 106:607–616. doi:10.1093/aob/mcq15
Van Staden J, Grobbelaar N (1995) The effect of sesbanimide and Sesbania seed extract on germination and seedling growth of a number of plant species. Environ Exp Bot 35:321–329. doi:10.1016/0098-8472(95)00005-0
Veronesi MB (2013) Avaliação da tolerância de duas espécies nativas às fitotoxinas exsudadas por Sesbania virgata (Cav.) Pers. Dissertation, Institute of Botany
Wang C-M, Li T-C, Jhan Y-L, Weng J-H, Chou C-H (2013) The impact of microbial biotransformation of catechin in enhancing the allelopathic effects of Rhododendron formosanum. PLoS ONE 8(12):e85162. doi:10.1371/journal.pone.0085162
Weidenhamer JD, Romeo JT (2005) Allelopathy as a mechanism for resisting invasion: the case of Polygonella myriophylla. Birkhauser, Basel, pp 167–177. doi:10.1007/3-7643-7380-6-10
Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19. doi:10.1016/S0305-1978(03)00085-1
Xuan TD, Elzaawely AA, Deba F, Fukuta M, Tawata S (2006) Mimosine in Leucaena as a potent bio-herbicide. Agron Sustain Dev 26:89–97. doi:10.1051/agro:2006001
Ye N, Zhu G, Liu Y, Zhang A, Li Y, Liu R, Shi L, Jia L, Zhang J (2011) Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. J Exp Bot 26:1–14. doi:10.1093/jxb/err336
Zanandrea I, Alves JD, Deuner S, Goulart PFP, Henrique PC, Silveira NM (2010) Tolerance of Sesbania virgata plants to flooding. Aust J Bot 57:661–669. doi:10.1071/BT09144
Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Braz J Bot 34:431–446. doi:10.1590/S0100-84042011000300016
Zhao H, Peng S, Chen Z, Wu Z, Zhou G, Wang X, Qiu Z (2011) Abscisic acid in soil facilitates community succession in three forests in China. J Chem Ecol 37:785–793. doi:10.1007/s10886-011-9970-z
Acknowledgements
We thank Dr. Luciano Freschi from University of São Paulo for the quantification of abscisic acid, Dr. Nelson Augusto dos Santos Junior for help with statistical analysis and critical review of the manuscript, and Dr. Maria Angela Machado de Carvalho for language revision and valuable suggestions. Thanks are due to Fundação de Amparo à Pesquisa de São Paulo—FAPESP for the fellowship to Daiane S.B. Mignoni (Proc 2013/03978-1) and for the financial support (Proc 2012/16332-0). Marcia R. Braga also thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq for the researcher fellowship and research grant (501965/2010-6).
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Mignoni, D.S.B., Simões, K. & Braga, M.R. Potential allelopathic effects of the tropical legume Sesbania virgata on the alien Leucaena leucocephala related to seed carbohydrate metabolism. Biol Invasions 20, 165–180 (2018). https://doi.org/10.1007/s10530-017-1524-z
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DOI: https://doi.org/10.1007/s10530-017-1524-z