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Mediterranean woody plant specialized metabolites affect germination of Linum perenne at its dry and upper thermal limits

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Abstract

Aims

Soil temperature and moisture impact plants not only during growth and survival but also during seed germination and interaction of seeds with the chemical environment. The quantitative impacts of either temperature and moisture or plant specialized metabolites (PSM) on germination are widely studied. However, the combined effect of PSM and moisture or temperature on germination remains poorly understood.

Methods

We addressed this issue by studying the effect of PSM extracted from four Mediterranean woody plants on germination speed and final percentages of a subordinate herbaceous plant, Linum perenne.

Results

By using hydro- and thermal time threshold models, we show how PSM interact with temperature and moisture levels to limit germination at dry and upper thermal limits, with the magnitude of effects depending on the source plant. PSM effects on germination, also observed on natural soils, persisted after their removal from the seed environment.

Conclusions

We conclude that the impact of climate change on reproduction of herbaceous plants can be modulated by effects of PSM from woody plants, which might exacerbate the negative impacts of global changes on biodiversity.

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References

  • Allemann I, Cawood ME, Allemann J (2016) Influence of abiotic stress on Amaranthus cruentus allelopathic properties. S Afr J Bot 306

    Google Scholar 

  • Anderson RC, Loucks OL (1966) Osmotic pressure influence in germination tests for antibiosis. Science 152:771–773

    CAS  PubMed  Google Scholar 

  • Arène F, Affre L, Doxa A, Saatkamp A (2017) Temperature but not moisture response of germination shows phylogenetic constraints while both interact with seed mass and life span. Seed Sci Res 27:110–120

    Google Scholar 

  • Benech-Arnold RL, Gualano N, Leymarie J, Côme D, Corbineau F (2006) Hypoxia interferes with ABA metabolism and increases ABA sensitivity in embryos of dormant barley grains. J Exp Bot 57:1423–1430

    CAS  PubMed  Google Scholar 

  • Blanco JA (2007) The representation of allelopathy in ecosystem-level forest models. Ecol Model 209:65–77

    Google Scholar 

  • Bogatek R, Gniazdowska A, Zakrzewska W, Oracz K, Gawronski SW (2006) Allelopathic effects of sunflower extracts on mustard seed germination and seedling growth. Biol Plant 50:156–158

    Google Scholar 

  • Bolker B (2017) Maximum likelihood estimation and analysis with the bbmle package

  • Bradford KJ (2002) Applications of hydrothermal time to quantifying and modeling seed germination and dormancy. Weed Sci 50:248–260

    CAS  Google Scholar 

  • Bradford KJ, Benech-Arnold RL, Côme D, Corbineau F (2008) Quantifying the sensitivity of barley seed germination to oxygen, abscisic acid, and gibberellin using a population-based threshold model. J Exp Bot 59:335–347

    CAS  PubMed  Google Scholar 

  • Briggs JS, Wall SBV, Jenkins SH (2009) Forest rodents provide directed dispersal of Jeffrey pine seeds. Ecology 90:675–687. https://doi.org/10.1890/07-0542.1

    Article  PubMed  Google Scholar 

  • Chomel M, Guittonny-Larchevêque M, Fernandez C, Gallet C, DesRochers A, Paré D, Jackson BG, Baldy V (2016) Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. J Ecol 104:1527–1541

    Google Scholar 

  • Courtois B, Olofsdotter M (1998) Incorporating the allelopathy trait in upland rice breeding programs. Allelopathy in Rice:57–68

  • Ehlers BK, Thompson J (2004) Do co-occurring plant species adapt to one another? The response of Bromus erectus to the presence of different Thymus vulgaris chemotypes. Oecologia 141:511–518

    PubMed  Google Scholar 

  • Einhellig FA (1989) Interactive effects of allelochemicals and environmental stress. Phytochemical Ecology: allelochemicals, mycotoxins and insect pheromones and allomones

  • Einhellig FA (1996) Interactions involving allelopathy in cropping systems. Agron J 88:886–893

    CAS  Google Scholar 

  • Einhellig FA, Eckrich PC (1984) Interactions of temperature and ferulic acid stress on grain sorghum and soybeans. J Chem Ecol 10:161–170

    CAS  PubMed  Google Scholar 

  • Fernandez C, Lelong B, Vila B, Mévy J-P, Robles C, Greff S, Dupouyet S, Bousquet-Mélou A (2006) Potential allelopathic effect of Pinus halepensis in the secondary succession: an experimental approach. Chemoecology 16:97–105. https://doi.org/10.1007/s00049-006-0334-z

    Article  CAS  Google Scholar 

  • Fernandez C, Santonja M, Gros R, Monnier Y, Chomel M, Baldy V, Bousquet-Mélou A (2013) Allelochemicals of Pinus halepensis as drivers of biodiversity in Mediterranean open mosaic habitats during the colonization stage of secondary succession. J Chem Ecol 39:298–311

    CAS  PubMed  Google Scholar 

  • Fernandez C, Monnier Y, Santonja M, Gallet C, Weston LA, Prévosto B, Saunier A, Baldy V, Bousquet-Mélou A (2016) The impact of competition and allelopathy on the trade-off between plant defense and growth in two contrasting tree species. Front Plant Sci 7:594–594

    PubMed  PubMed Central  Google Scholar 

  • Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977–977

    CAS  PubMed  Google Scholar 

  • Gatti AB, Takao LK, Pereira VC, Ferreira AG, Lima MIS, Gualtieri SCJ (2014) Seasonality effect on the allelopathy of cerrado species. Braz J Biol 74:S064–S069

    Google Scholar 

  • Gavinet J, Prévosto B, Bousquet-Mélou A, Gros R, Quer E, Baldy V, Fernandez C (2018) Do litter-mediated plant-soil feedbacks influence Mediterranean oak regeneration? A two-year pot experiment. Plant Soil 430:59–71

    CAS  Google Scholar 

  • Gavinet J, Santonja M, Baldy V, Hashoum H, Peano S, Tchong T, Gros R, Greff S, Fernandez C, Bousquet-Mélou A (2019) Phenolics of the understory shrub Cotinus coggygria influence Mediterranean oak forests diversity and dynamics. For Ecol Manag 441:262–270

    Google Scholar 

  • Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Glob Planet Chang 63:90–104

    Google Scholar 

  • Hashoum H, Santonja M, Gauquelin T, Saatkamp A, Gavinet J, Greff S, Lecareux C, Fernandez C, Bousquet-Mélou A (2017) Biotic interactions in a Mediterranean oak forest: role of allelopathy along phenological development of woody species. Eur J For Res 136:699–710

    Google Scholar 

  • Herranz JM, Ferrandis P, Copete MA, Duro EM, Zalacaín A (2006) Effect of allelopathic compounds produced by Cistus ladanifer on germination of 20 Mediterranean taxa. Plant Ecol 184: 259–272

    Google Scholar 

  • Hoerling M, Eischeid J, Perlwitz J, Quan X, Zhang T, Pegion P (2012) On the increased frequency of Mediterranean drought. J Clim 25:2146–2161

    Google Scholar 

  • Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008) Post-genomics dissection of seed dormancy and germination. Trends Plant Sci 13:7–13

    CAS  PubMed  Google Scholar 

  • Huang Z, Liu S, Bradford KJ, Huxman TE, Venable DL (2016) The contribution of germination functional traits to population dynamics of a desert plant community. Ecology 97:250–261

    PubMed  Google Scholar 

  • IUSS Working Group WRB (2006) World reference base for soil resources. World Soil Resources Report 103

  • Jefferson L, Pennacchio M (2003) Allelopathic effects of foliage extracts from four Chenopodiaceae species on seed germination. J Arid Environ 55:275–285

    Google Scholar 

  • Kaya Y, Aksakal O, Sunar S, Erturk FA, Bozari S, Agar G, Erez ME, Battal P (2015) Phytotoxical effect of Lepidium draba L. extracts on the germination and growth of monocot (Zea mays L.) and dicot (Amaranthus retroflexus L.) seeds. Toxicol Ind Health 31:247–254

    CAS  PubMed  Google Scholar 

  • Klanderud K (2005) Climate change effects on species interactions in an alpine plant community. J Ecol 93:127–137

    Google Scholar 

  • Kobayashi K (2004) Factors affecting phytotoxic activity of allelochemicals in soil. Weed Biol Manage 4:1–7

    CAS  Google Scholar 

  • Kruse M, Strandberg M, Strandberg B (2000) Ecological effects of allelopathic plants-a review. NERI Technical Report 315

  • Liptay A, Schopfer P (1983) Effect of water stress, seed coat restraint, and abscisic acid upon different germination capabilities of two tomato lines at low temperature. Plant Physiol 73:935–938

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lobón NC, Gallego JCA, Diaz TS, Garcia JCE (2002) Allelopathic potential of Cistus ladanifer chemicals in response to variations of light and temperature. Chemoecology 12:139–145

    Google Scholar 

  • Ma Z, Fang T, Thring RW, Li Y, Yu H, Zhou Q, Zhao M (2015) Toxic and non-toxic strains of Microcystis aeruginosa induce temperature dependent allelopathy toward growth and photosynthesis of Chlorella vulgaris. Harmful Algae 48:21–29

    CAS  PubMed  Google Scholar 

  • Melkania NP (1992) Allelopathy in forest and agroecosystems in the Himalayan region. Springer, Allelopathy

    Google Scholar 

  • Michel BE (1983) Evaluation of the water potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiol 72:66–70

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ni BR, Bradford KJ (1992) Quantitative models characterizing seed germination responses to abscisic acid and osmoticum. Plant Physiol 98:1057–1068

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oueslati O, Ben-Hammouda M, Ghorbal MH, Guezzah M, Kremer RJ (2005) Barley autotoxicity as influenced by varietal and seasonal variation. J Agron Crop Sci 191:249–254

    Google Scholar 

  • Pedrol N, González L, Reigosa MJ (2006) Allelopathy and abiotic stress. In Allelopathy (pp. 171-209). Springer, Dordrecht

  • Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483. https://doi.org/10.1111/j.1461-0248.2011.01609.x

    Article  PubMed  Google Scholar 

  • Rice EL (1984) Allelopathy, New York

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450

    PubMed  Google Scholar 

  • Ruan X, Pan CD, Liu R, Li ZH, Li SL, Jiang DA, Zhang JC, Wang G, Zhao YX, Wang Q (2016) Effects of climate warming on plant autotoxicity in forest evolution: a case simulation analysis for Picea schrenkiana regeneration. Ecol Evol 6:5854–5866

    PubMed  PubMed Central  Google Scholar 

  • Ruprecht E, Donath TW, Otte A, Eckstein RL (2008) Chemical effects of a dominant grass on seed germination of four familial pairs of dry grassland species. Seed Sci Res 18:239–248

    Google Scholar 

  • Saatkamp A, Affre L, Dutoit T, Poschlod P (2011) Germination traits explain soil seed persistence across species: the case of Mediterranean annual plants in cereal fields. Ann Bot 107:415–415

    PubMed  PubMed Central  Google Scholar 

  • Saatkamp A, Cochrane A, Commander L, Guja LK, Jimenez-Alfaro B, Larson J, Nicotra A, Poschlod P, Silveira FA, Cross AT, Dalziell EL, Dickie J, E ET, Fidelis A, Fuchs A, Golos PJ, Hope M, Lewandrowski W, Meritt DJ, Miller BP, Miller RG, Offord CA, Ooi MKJ, Satyantis A, Sommerville KD, Tangney R, Tomlinson S, Turner S, Walck JL (2019) A research agenda for seed-trait functional ecology. New Phytol 221:1764–1775

    PubMed  Google Scholar 

  • Schopfer P, Plachy C (1984) Control of seed germination by abscisic acid: II. Effect on embryo water uptake in Brassica napus L. Plant Physiol 76:155–160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scognamiglio M, D’Abrosca B, Esposito A, Pacifico S, Monaco P, Fiorentino A (2013) Plant growth inhibitors: allelopathic role or phytotoxic effects? Focus on Mediterranean biomes. Phytochem Rev 12:803–830

    CAS  Google Scholar 

  • Shaw LJ, Morris P, Hooker JE (2006) Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ Microbiol 8:1867–1880. https://doi.org/10.1111/j.1462-2920.2006.01141.x

    Article  CAS  PubMed  Google Scholar 

  • Souto XC, Gonzales L, Reigosa MJ (1994) Comparative analysis of allelopathic effects produced by four forestry species during decomposition process in their soils in Galicia (NW Spain). J Chem Ecol 20:3005–3015

    CAS  PubMed  Google Scholar 

  • Souto XC, Bolaño JC, González L, Reigosa M (2001) Allelopathic effects of tree species on some soil microbial populations and herbaceous plants. Biol Plant 44:269–275

    Google Scholar 

  • Terzi I, Kocaçalişkan İ (2010) The effects of gibberellic acid and kinetin on overcoming the effects of juglone stress on seed germination and seedling growth. Turk J Bot 34:67–72

    Google Scholar 

  • Turker M, Battal P, Agar G, Gulluce M, Sahin F, Erez M, Yildirim N (2008) Allelopathic effects of plants extracts on physiological and cytological processes during maize seed germination. Allelopath J 21:273

    Google Scholar 

  • Vesty EF, Saidi Y, Moody LA, Holloway D, Whitbread A, Needs S, Choudhary A, Burns B, McLeod D, Bradshaw SJ, Bae H, King BC, Bassel GW, Simonsen HT, Coates JC (2016) The decision to germinate is regulated by divergent molecular networks in spores and seeds. New Phytol 211:952–966. https://doi.org/10.1111/nph.14018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vyvyan JR (2002) Allelochemicals as leads for new herbicides and agrochemicals. Tetrahedron 58:1631–1646

    CAS  Google Scholar 

  • Wang R-L, Zeng R-S, Peng S-L, Chen B-M, Liang X-T, Xin X-W (2011) Elevated temperature may accelerate invasive expansion of the liana plant Ipomoea cairica. Weed Res 51:574–580

    Google Scholar 

  • Williams DH, Stone MJ, Hauck PR, Rahman SK (1989) Why are secondary metabolites (natural products) biosynthesized? J Nat Prod 52:1189–1208

    CAS  PubMed  Google Scholar 

  • Yang L, Ruan X, Jiang D, Zhang J, Pan C, Wang Q (2017) Physiological effects of autotoxicity due to DHAP stress on Picea schrenkiana regeneration. PLoS One 12:e0177047

    PubMed  PubMed Central  Google Scholar 

  • Zhang J, Wang Y, Yang T, Jin H, Zhang J (2012) Use of gibberellic acid to overcome the allelopathic effect of a range of species on the germination of seeds of Gentiana rigescens, a medicinal herb. Seed Sci Technol 40:443–447

    Google Scholar 

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Acknowledgments

This study was supported by the grant ANR-12-BSV7-0016-01 of the French Agence Nationale pour la Recherche through the project SecPriMe2 to CF, the Région Provence Alpes Côte d’Azur supported this work through its Gévoclé grant to AS. The OHP site belongs to SOERE F-ORE-T, and SOERE TEMPO supported by Ecofor, Allenvi and the French national research infrastructure, ANAEE-F, www.anaee-france.fr.

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Author notes

  1. Hazem Hashoum and Arne Saatkamp contributed equally to this work.

Authors and Affiliations

  1. Aix Marseille Université, IMBE UMR 7263, CNRS, IRD, Avignon Université, Marseille, France

    Hazem Hashoum & Arne Saatkamp

Authors
  1. Hazem Hashoum
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  2. Arne Saatkamp
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  3. Thierry Gauquelin
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  4. Julien Ruffault
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  5. Catherine Fernandez
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  6. Anne Bousquet-Mélou
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Contributions

• HH, AS, TG, CF and ABM conceived and designed the research;

• HH and AS collected the data;

• HH and AS analyzed and interpreted the data;

• HH, AS, led the writing and HH, AS, TG, CF, JR, ABM revised the manuscript.

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Correspondence to Arne Saatkamp.

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Hashoum, H., Saatkamp, A., Gauquelin, T. et al. Mediterranean woody plant specialized metabolites affect germination of Linum perenne at its dry and upper thermal limits. Plant Soil 446, 291–305 (2020). https://doi.org/10.1007/s11104-019-04366-6

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  • DOI: https://doi.org/10.1007/s11104-019-04366-6

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