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Extreme drought alters progeny dispersal unit properties of winter wild oat (Avena sterilis L.)

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Abstract

Main conclusion

The dead husk is a vital component of the dispersal unit whose biochemical properties can be modified following exposure to drought. This might affect seed performance and fate, soil properties and consequently plant biodiversity.

Abstract

We investigated the effects of extreme drought on the dispersal unit (DU) properties of winter wild oat (Avena sterilis L.) in the Mediterranean ecosystems focusing on a commonly ignored component of the DU, namely the dead floral bracts (husk). DUs were collected from a climate change experimental research station in the Judean Hills, Israel, simulating extreme drought and from two additional sites differing in the rainfall amounts. Our results showed that drought conditions significantly affected A. sterilis reproductive traits displaying reduced DUs and caryopses weights. The husk contributes profoundly to seed performance showing that germination from the intact DUs or the intact florets 1 was higher, faster and more homogenous compared to naked caryopses; no effect of drought on germination properties was observed. The husk stored hundreds of proteins that retain enzymatic activity and multiple metabolites including phytohormones. Changes in rainfall amounts affected the composition and levels of proteins and other metabolites accumulated in the husk, with a notable effect on abscisic acid (ABA). The husk of both control and drought plants released upon hydration substances that selectively inhibited other species seed germination as well as substances that promoted microbial growth. Our data showed that the dead husk represents a functional component of the DU that have been evolved to nurture the embryo and to ensure its success in its unique habitat. Furthermore, drought conditions can modify husk biochemical properties, which in turn might affect seed performance and fate, soil microbiota and soil fertility and consequently plant species diversity.

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Abbreviations

DOEE:

Dead organs enclosing embryo

DU:

Dispersal unit

JA:

Jasmonic acid

LTER:

Long-term ecological research

SA:

Salicylic acid

References

  • Adkins SW, Bellairs SM, Loch DS (2002) Seed dormancy mechanisms in warm season grass species. Euphytica 126:13–20

    CAS  Google Scholar 

  • Alon M, Sternberg M (2019) Effects of extreme drought on primary production, species composition and species diversity of a Mediterranean annual plant community. J Veg Sci 30:1045–1061

    Google Scholar 

  • Arnaiz A, Talavera-Mateo L, Gonzalez-Melendi P, Martinez M, Diaz I, Santamaria ME (2018) Arabidopsis Kunitz trypsin inhibitors in defense against spider mites. Front Plant Sci 9:986

    Google Scholar 

  • Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26

    Google Scholar 

  • Booth DT, Schuman GE (1983) Seedbed ecology of winterfat: fruits versus threshed seeds. J Range Manag 38:387–390

    Google Scholar 

  • Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres L, Kunstler G, Liancourt P, Tielbörger K, Travis JMJ, Anthelme F et al (2008) Facilitation in plant communities: the past, the present and the future. J Ecol 96:18–34

    Google Scholar 

  • Chandrashekar N, Ali S, Grover A (2018) Exploring expression patterns of PR-1, PR-2, PR-3, and PR-12 like genes in Arabidopsis thaliana upon Alternaria brassicae inoculation. Biotechnology 8:230

    CAS  Google Scholar 

  • Cousens RD, Young KR, Tadayyon A (2010) The role of the persistent fruit wall in seed water regulation in Raphanus raphanistrum (Brassicaceae). Ann Bot 105:101–108

    Google Scholar 

  • Doungous O, Minyaka E, Longue EAM, Nkengafac NJ (2018) Potentials of cocoa pod husk-based compost on Phytophthora pod rot disease suppression, soil fertility, and Theobroma cacao L. growth. Environ Sci Pollut Res 25:25327–25335

    CAS  Google Scholar 

  • Elbaum R, Zaltzman L, Burgert I, Fratzl P (2007) The role of wheat awns in the seed dispersal unit. Science 316:884–886

    CAS  Google Scholar 

  • El-Keblawy A, Elgabra M, Mosa KA, Fakhry A, Soliman S (2019) Roles of hardened husks and membranes surrounding Brachypodium hybridum grains on germination and seedling growth. Plants 8:322

    CAS  Google Scholar 

  • Evenari M (1949) Germination inhibitors. Bot Rev 15:153–194

    Google Scholar 

  • Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol 150:1750–1761

    CAS  Google Scholar 

  • Fandrich L, Mallory-Smith CA (2006) Factors affecting germination of jointed goatgrass (Aegilops cylindrica) seed. Weed Sci 54:677–684

    CAS  Google Scholar 

  • Feinbrun-Dothan N, Danin A (1998) Analytical flora of Eretz-Israel. Plitmann U (ed). CANA Publishing House Ltd, Jerusalem

  • Fenner M (1991) The effects of the parent environment on seed germinability. Seed Sci Res 1:75–84

    Google Scholar 

  • Finch-Savage WE, Bassel GW (2016) Seed vigour and crop establishment: extending performance beyond adaptation. J Exp Bot 67:567–591

    CAS  Google Scholar 

  • Fukumoto K, Md AK, Yamashita Y, Mori IC, Matsuura H, Galis I (2013) Response of rice to insect elicitors and the role of OsJAR1 in wound and herbivory-induced JA-Ile accumulation. J Integr Plant Biol 55:775–784

    CAS  Google Scholar 

  • Godwin J, Raviv B, Grafi G (2017) Dead pericarps of dry fruits function as long-term storage for active hydrolytic enzymes and other substances that affect germination and microbial growth. Plants (Basel) 6:64

    Google Scholar 

  • Golodets C, Sternberg M, Kigel J, Boeken B, Henkin Z, Seligman NG, Ungar EU (2015) Climate change scenarios of biomass production along an aridity gradient: vulnerability increases with aridity. Oecologia 177:971–979

    Google Scholar 

  • Granot G, Morgenstern Y, Khan A, Rapp YG, Pesok A, Nevo E, Grafi G (2015) Internucleosomal DNA fragmentation in wild emmer wheat is catalyzed by S1-type endonucleases translocated to the nucleus upon induction of cell death. Biochim Biophys Acta 1849:239–246

    CAS  Google Scholar 

  • Grover A (2012) Plant chitinases: genetic diversity and physiological roles. Crit Rev Plant Sci 31:57–73

    CAS  Google Scholar 

  • Gutterman Y (2000) Maternal effects on plants during development. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI Publishing, Wallingford, pp 59–84

    Google Scholar 

  • Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22:534–543

    Google Scholar 

  • Hendrix SD (1984) Variation in seed weight and its effects on germination in Pastinaca sativa L (Umbelliferae). Am J Bot 71:795–802

    Google Scholar 

  • Hu XW, Wang YR, Wu YP (2009) Effects of the pericarp on imbibition, seed germination, and seedling establishment in seeds of Hedysarum scoparium Fisch. et Mey. Ecol Res 24:559–564

    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

    Google Scholar 

  • Hugot K, Ponchet M, Marais A, Ricci P, Galiana E (2002) A tobacco S-like RNase inhibits hyphal elongation of plant pathogens. Mol Plant Microbe Interact 15:243–250

    CAS  Google Scholar 

  • IPCC (2018) Global Warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. Masson-Delmotte V, Zhai P, Pörtner H-O, Roberts D, et al. (eds.)

  • Kader MA (2005) A comparison of seed germination calculation formulae and the associated interpretation of resulting data. J Proc R Soc NSW 138:65–75

    Google Scholar 

  • Kawaguchi S, Yoneyama K, Yokota T, Takeuchi Y, Ogasawara M, Konnai M (1997) Effects of aqueous extract of rice plants (Oryza sativa L.) on seed germination and radicle elongation of Monochoria vaginalis var. plantaginea. Plant Growth Regul 23:183–189

    CAS  Google Scholar 

  • Khadka J, Raviv B, Swetha B, Grandhi R, Singiri JR, Novoplansky N, Gutterman Y, Galis I, Huang Z, Grafi G (2020) Maternal environment alters dead pericarp biochemical properties of the desert annual plant Anastatica hierochuntica L. PLoS ONE 15:e0237045

    CAS  Google Scholar 

  • Kremer RJ (1986) Antimicrobial activity of velvetleaf (Abutilon theophrasti) seeds. Weed Sci 34:617–622

    Google Scholar 

  • Kushima M, Kakuta H, Kosemura S, Yamamura S, Yamada K, Yokotani-Tomita K, Hasegawa K (1998) An allelopathic substance exuded from germinating watermelon seeds. Plant Growth Regul 25:1–4

    CAS  Google Scholar 

  • Lamkemeyer P, Laxa M, Collin V, Li W, Finkemeier I, Schöttler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, Kandlbinder A et al (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968–981

    CAS  Google Scholar 

  • Li YP, Ye W, Wang M, Yan XD (2009) Climate change and drought: a risk assessment of crop-yield impacts. Clim Res 39:31–46

    CAS  Google Scholar 

  • Lionello P, Abrantes F, Gacic M, Planton S, Trigo R, Ulbrich U (2014) The climate of the Mediterranean region: research progress and climate change impacts. Reg Environ Change 14:1679–1684

    Google Scholar 

  • Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry–based metabolite profiling in plants. Nat Protoc 1:387

    CAS  Google Scholar 

  • Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449

    CAS  Google Scholar 

  • Mamut J, Tan DY, Baskin CC, Baskin JM (2014) Role of trichomes and pericarp in the seed biology of the desert annual Lachnoloma lehmannii (Brassicaceae). Ecol Res 29:33–44

    Google Scholar 

  • Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68: 485–512

    CAS  Google Scholar 

  • Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8:409–414

    CAS  Google Scholar 

  • McIntyre PJ, Thorne JH, Dolanc CR, Flint AL, Flint LE, Kelly M, Ackerly DD (2015) Twentieth-century shifts in forest structure in California: denser forests, smaller trees, and increased dominance of oaks. Proc Natl Acad Sci USA 112:1458–1463

    CAS  Google Scholar 

  • Miyajima D (1996) Germination of zinnia seed with and without pericarp. Seed Sci Technol 24:465–473

    Google Scholar 

  • Nave M, Avni R, Ben-Zvi B, Hale I, Distelfeld A (2016) QTLs for uniform grain dimensions and germination selected during wheat domestication are co-located on chromosome 4B. Theor Appl Genet 129:1303–1315

    CAS  Google Scholar 

  • Ogawa K, Iwabuchi M (2001) A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide. Plant Cell Physiol 42:286–291

    CAS  Google Scholar 

  • Ohno S, Tomita-Yokotani K, Kosemura S, Node M, Suzuki T, Amano M, Yasui K, Goto T, Yamamura S, Hasegawa K (2001) A species-selective allelopathic substance from germinating sunflower (Helianthus annuus L.) seeds. Phytochemistry 56:577–581

    CAS  Google Scholar 

  • Patton T, Barrett J, Brennan J, Moran N (2006) Use of a spectrophotometric bioassay for determination of microbial sensitivity to manuka honey. J Microbiol Methods 64:84–95

    CAS  Google Scholar 

  • Penfield S, MacGregor DR (2017) Effects of environmental variation during seed production on seed dormancy and germination. J Exp Biol 68:819–825

    CAS  Google Scholar 

  • Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

    CAS  Google Scholar 

  • Prakash A, Nithyanand P, Vadivel V (2018) In vitro antibacterial activity of nut by-products against foodborne pathogens and their application in fresh-cut fruit model. J Food Sci Technol 55:4304–4310

    CAS  Google Scholar 

  • Raviv B, Granot G, Chalifa-Caspi V, Grafi G (2017a) The dead, hardened floral bracts of dispersal units of wild wheat function as storage for active hydrolases and in enhancing seedling vigor. PLoS ONE 12:e0177537

    Google Scholar 

  • Raviv B, Aghajanyan L, Granot G, Makover V, Frenkel O, Gutterman Y, Grafi G (2017b) The dead seed coat functions as a long-term storage for active hydrolytic enzymes. PLoS ONE 12:e0181102

    Google Scholar 

  • Raviv B, Godwin J, Granot G, Grafi G (2018) The dead can nurture: novel insights into the function of dead organs enclosing embryos. Int J Mol Sci 19:2455

    Google Scholar 

  • Richards SL, Wilkins KA, Swarbreck SM, Anderson AA, Habib N, Smith AG, McAinsh M, Davies JM (2015) The hydroxyl radical in plants: from seed to seed. J Exp Bot 66:37–46

    CAS  Google Scholar 

  • Rodríguez-Gacio Mdel C, Matilla-Vázquez MA, Matilla AJ (2009) Seed dormancy and ABA signaling: the breakthrough goes on. Plant Signal Behav 4:1035–1049

    Google Scholar 

  • Román-Palacios C, Wiens JJ (2020) Recent responses to climate change reveal the drivers of species extinction and survival. Proc Natl Acad Sci USA 117:4211–4217

    Google Scholar 

  • Sankary MN, Barbour MG (1972) Autecology of Atriplex polycarpa from California. Ecology 53:1155–1162

    Google Scholar 

  • Sari A, Oguz B, Bilgic A (2006) Breaking seed dormancy of laurel (Laurus nobilis L.). New For 31:403–408

    Google Scholar 

  • Scheler C, Weitbrecht K, Pearce SP, Hampstead A, Büttner-Mainik A, Lee KJ, Voegele A, Oracz K, Dekkers BJ, Wang X et al (2015) Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases. Plant Physiol 167:200–215

    CAS  Google Scholar 

  • Sharma N, Sharma KP, Gaur RK, Gupta VK (2011) Role of chitinase in plant defense. Asian J Biochem 6:29–37

    CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  Google Scholar 

  • Spinoni J, Naumann G, Carrao H, Barbosa P, Vogt J (2014) World drought frequency, duration, and severity for 1951–2010. Int J Climatol 34:2792–2804

    Google Scholar 

  • Sternberg T (2011) Regional drought has a global impact. Nature 472: 169

    CAS  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    CAS  Google Scholar 

  • Ueno, Miyoshi K (2005) Difference of optimum germination temperature of seeds of intact and dehusked japonica rice during seed development. Euphytica 143:271–275

    Google Scholar 

  • Vandvik V, Klanderud K, Meineri E, Måren IE, Töpper J (2015) Seed banks are biodiversity reservoirs: species-area relationships above versus below ground. Oikos 125:218–228

    Google Scholar 

  • Volis S (2014) Dormancy-related seed positional effect in two populations of an annual grass from locations of contrasting aridity. PLoS ONE 9:e93061

    Google Scholar 

  • Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P (2011) Climate change and plant regeneration from seed. Global Change Biol 17:2145–2161

    Google Scholar 

  • Wang Z, Zhao Y, Zhang Y, Zhao B, Yang Z, Dong L (2019) The role of seed appendage in improving the adaptation of a species in definite seasons: a case study of Atriplex centralasiatica. BMC Plant Biol 19:538

    Google Scholar 

  • Watson TG (1975) Inhibition of microbial fermentations by sorghum grain and malt. J Appl Microbiol 38:133–142

    CAS  Google Scholar 

  • Webb J, Miao S, Zhang X-H (2009) Factors and mechanisms influencing seed germination in a wetland plant sawgrass. Plant Growth Regul 57:243–250

    CAS  Google Scholar 

  • Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ (2012) Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot 63:3499–3509

    CAS  Google Scholar 

  • Worrall D, Holroyd GH, Moore JP, Glowacz M, Croft P, Taylor JE, Paul ND, Roberts MR (2012) Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytol 193:770–778

    CAS  Google Scholar 

  • Wurzburger J, Leshem Y (1969) Physiological action of the germination inhibitor in the husk of Aegilops kotschyi Boiss. New Phytol 68:337–341

    Google Scholar 

  • Xuejun Y, Baskin J, Baskin C, Huang Z (2012) More than just a coating: ecological importance, taxonomic occurrence and phylogenetic relationships of seed coat mucilage. Perspect Plant Ecol 14:434–442

    Google Scholar 

  • Yi F, Wang Z, Baskin CC, Baskin JM, Ye R, Sun H, Zhang Y, Ye X, Liu G, Yang X, Huang Z (2019) Seed germination responses to seasonal temperature and drought stress are species-specific but not related to seed size in a desert steppe: Implications for effect of climate change on community structure. Ecol Evol 9:2149–2159

    Google Scholar 

  • Zhang J, Maun MA (1990) Seed size variation and its effects on seedling growth in Agropyron psammophilum. Bot Gaz 151:106–113

    Google Scholar 

  • Ziv B, Saaroni H, Pargament R, Harpaz T, Alpert P (2014) Trends in rainfall regime over Israel, 1975–2010, and their relationship to large-scale variability. Reg Environ Change 14:1751–1764

    Google Scholar 

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Acknowledgements

The work was supported by the NSFC-ISF Research Grant (Grant No. 2456/18 to G.G.) and by the Israeli Ministry of Science and Technology (MOST) (Grant No. 61208 to M.S; ORCID Number: 0000-0001-8710-4141). This work was partly supported by the Joint Usage/Research Center, Institute of Plant Science and Resources, Okayama University, Japan.

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Author notes

  1. Buzi Raviv, Janardan Khadka and Bupur Swetha contributed equally.

Authors and Affiliations

  1. French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990, Midreshet Ben Gurion, Israel

    Buzi Raviv, Janardan Khadka, Bupur Swetha, Jeevan R. Singiri, Rohith Grandhi, Eliyahu Shapira, Nurit Novoplansky, Yitzchak Gutterman & Gideon Grafi

  2. Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama, 710-0046, Japan

    Ivan Galis

  3. School of Plant Sciences and Food Security, Wise Faculty of Life Sciences, Tel Aviv University, 69978, Tel Aviv, Israel

    Marcelo Sternberg

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  1. Buzi Raviv
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  2. Janardan Khadka
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  3. Bupur Swetha
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Correspondence to Gideon Grafi.

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Raviv, B., Khadka, J., Swetha, B. et al. Extreme drought alters progeny dispersal unit properties of winter wild oat (Avena sterilis L.). Planta 252, 77 (2020). https://doi.org/10.1007/s00425-020-03491-2

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