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Seeds vs fungi: an enzymatic battle in the soil seedbank

Published online by Cambridge University Press:  05 June 2018

Anne T. Pollard*
Affiliation:
Department of Crop and Soil Sciences, Washington State University, PO Box 646420, Pullman, WA 99164-6420, USA
*
Author for correspondence: Anne T. Pollard Email: anne.pollard@wsu.edu

Abstract

Depleting the soil weed seedbank is an important integrated weed management strategy that has the potential to foster lasting weed control. Long-term dormancy and decay resistance of weed seeds pose a challenge to weed eradication efforts. Select soil fungi have been shown to cause significant decay of weed seeds. The physical and chemical mechanisms by which seeds in the seedbank defend themselves against pathogens have been well researched. However, very few studies have purposefully investigated the biochemical defence response of seeds. Enzyme-based biochemical seed defences have been detected in dormant and non-dormant seeds, and research supports their function in pathogen defence. This review summarizes current knowledge of the seed defence enzymes polyphenol oxidase, peroxidase, chitinase and oxalate oxidase. The fungal enzymes chitinase, protease and xylanase that function in pathogenesis of seeds in the soil seedbank are also reviewed. Progress in the development and standardization of in situ enzyme analyses fosters our understanding of actual enzyme activity present in soils, while high-throughput microplate techniques promote efficiency and enable greater scope. Application of genomic, proteomic and transcriptomic techniques to glean a deeper and more holistic understanding of the enzymatic interactions of weed seeds and soil fungi in the soil seedbank will support the development of improved integrated weed management strategies.

Type
Review Paper
Copyright
Copyright © Cambridge University Press 2018 

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References

Abidi, F, Limam, F and Marzouki, MN (2007) Purification and characterization of an alkaline protease prot 1 from Botrytis cinerea. Applied Biochemistry and Biotechnology 141, 361376.Google Scholar
Adrangi, S and Faramarzi, MA (2013) From bacteria to human: a journey into the world of chitinases. Biotechnology Advances 31, 17861795.Google Scholar
Akbar, N, Jabran, K and Ali, MA (2011) Weed management improves yield and quality of direct seeded rice. Australian Journal of Crop Science 5, 688694.Google Scholar
Almagro, L et al. (2009) Class III peroxidases in plant defence reactions. Journal of Experimental Botany 60, 377390.Google Scholar
Alvarez, ME et al. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773784.Google Scholar
Anderson, JV et al. (2010) Activation of polyphenol oxidase in dormant wild oat caryopses by a seed-decay isolate of Fusarium avenaceum. Journal of Agricultural and Food Chemistry 58, 1059710605.Google Scholar
Aniszewski, T, Lieberei, R and Gulewicz, K (2008) Research on catecholases, laccases and cresolases in plants. Recent progress and future needs. Acta Biologica Cracoviensia Series Botanica 50, 718.Google Scholar
Arimori, T et al. (2013) Crystal structures of the catalytic domain of a novel glycohydrolase family 23 chitinase from Ralstonia sp. A-471 reveals a unique arrangement of the catalytic residues for inverting chitin hydrolysis. Journal of Biological Chemistry 288, 1869618706.Google Scholar
Aybeke, M, Şen, B and Ökten, S (2014) Aspergillus alliaceus, a new potential biological control of the root parasitic weed Orobanche. Journal of Basic Microbiology 54, S93101.Google Scholar
Bach, CE et al. (2013) Measuring phenol oxidase and peroxidase activities with pyrogallol, L-DOPA, and ABTS: effect of assay conditions and soil type. Soil Biology and Biochemistry 67, 183191.Google Scholar
Baek, JH, Han, BK and Jo, DH (2001) Distribution of chitinases in rice (Oryza sativa L.) seed and characterization of a hull-specific chitinase. BMB Reports 34, 310315.Google Scholar
Baldrian, P (2006) Fungal laccases – occurrence and properties. FEMS Microbiology Reviews 30, 215242.Google Scholar
Banci, L (1997) Structural properties of peroxidases. Journal of Biotechnology 53, 253263.Google Scholar
Barceló, AR et al. (2003) Peroxidase: a multifunctional enzyme in grapevines. Functional Plant Biology 30, 577591.Google Scholar
Barman, AR and Banerjee, J (2015) Versatility of germin-like proteins in their sequences, expressions, and functions. Functional and Integrative Genomics 15, 533548.Google Scholar
Baskin, CC and Baskin, JM (2006) The natural history of soil seed banks of arable land. Weed Science 54, 549557.Google Scholar
Baskin, CC and Baskin, JM (2014) Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. San Diego, CA: Elsevier, Academic Press.Google Scholar
Baskin, JM and Baskin, CC (1985) The annual dormancy cycle in buried weed seeds: a continuum. BioScience 35, 492498.Google Scholar
Bastiaans, L, Paolini, R and Baumann, DT (2008) Focus on ecological weed management: what is hindering adoption? Weed Research 48, 481491.Google Scholar
Beaugrand, J et al. (2004) Impact and efficiency of GH10 and GH11 thermostable endoxylanases on wheat bran and alkali-extractable arabinoxylans. Carbohydrate Research 339, 25292540.Google Scholar
Beckie, HJ, Francis, A and Hall, LM (2012) The biology of Canadian weeds. 27. Avena fatua L. (updated). Canadian Journal of Plant Science 92, 13291357.Google Scholar
Beckstead, J et al. (2007) A race for survival: can Bromus tectorum seeds escape Pyrenophora semeniperda-caused mortality by germinating quickly? Annals of Botany 99, 907914.Google Scholar
Benech-Arnold, RL et al. (2000) Environmental control of dormancy in weed seed banks in soil. Field Crops Research 67(2), 105122.Google Scholar
Berendsen, RL, Pieterse, CM and Bakker, PA (2012) The rhizosphere microbiome and plant health. Trends in Plant Science 17, 478486.Google Scholar
Bhatt, I and Tripathi, BN (2011) Plant peroxiredoxins: catalytic mechanisms, functional significance and future perspectives. Biotechnology Advances 29, 850859.Google Scholar
Bolingue, W et al. (2010) The MtSNF4b subunit of the sucrose non-fermenting-related kinase complex connects after-ripening and constitutive defense responses in seeds of Medicago truncatula. The Plant Journal 61, 792803.Google Scholar
Brito, N, Espino, JJ and González, C (2006) The endo-β-1, 4-xylanase Xyn11A is required for virulence in Botrytis cinerea. Molecular Plant–Microbe Interactions 19, 2532.Google Scholar
Broekaert, WF et al. (1995) Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiology 108, 13531358.Google Scholar
Buhler, DD (2002) 50th Anniversary – Invited Article: Challenges and opportunities for integrated weed management. Weed Science 50, 273280.Google Scholar
Buhler, DD, Hartzler, RG and Forcella, F (1997) Weed seed bank dynamics: implications to weed management. Journal of Crop Production 1, 145168.Google Scholar
Burns, RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biology and Biochemistry 14, 423427.Google Scholar
Burns, RG et al. (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology and Biochemistry 58, 216234.Google Scholar
Bykova, NV et al. (2011) Redox-sensitive proteome and antioxidant strategies in wheat seed dormancy control. Proteomics 11, 865882.Google Scholar
Cadman, CS et al. (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. The Plant Journal 46, 805822.Google Scholar
Cai, Y et al. (2013) Genome-wide analysis of polyphenol oxidase genes and their transcriptional patterns during grain development in sorghum. International Journal of Plant Sciences 174, 710721.Google Scholar
Carrillo, MGC et al. (2009) Phylogenomic relationships of rice oxalate oxidases to the cupin superfamily and their association with disease resistance QTL. Rice 2, 6779.Google Scholar
Chandrasekaran, M et al. (2016) Proteases from phytopathogenic fungi and their importance in phytopathogenicity. Journal of General Plant Pathology 82, 233239.Google Scholar
Chang, YM et al. (2014) Characterization of an acidic chitinase from seeds of black soybean (Glycine max (L) Merr Tainan No. 3). PloS One 9, p.e113596.Google Scholar
Charudattan, R (1991) The mycoherbicide approach with plant pathogens. In Microbial Control of Weeds. Springer US, pp. 2457.Google Scholar
Chee-Sanford, JC (2008) Weed seeds as nutritional resources for soil Ascomycota and characterization of specific associations between plant and fungal species. Biology and Fertility of Soils 44, 763771.Google Scholar
Chee-Sanford, J and Fu, X (2010) Investigating the role of microorganisms in soil seed bank management. Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology 1, 257266.Google Scholar
Chikowo, R et al. (2009) Integrated weed management systems allow reduced reliance on herbicides and long-term weed control. Agriculture, Ecosystems and Environment 132, 237242.Google Scholar
Chrispeels, MJ (1991) Sorting of proteins in the secretory system. Annual Review of Plant Biology 42, 2153.Google Scholar
Chrispeels, MJ and Raikhel, NV (1991) Lectins, lectin genes, and their role in plant defense. The Plant Cell 3, 19.Google Scholar
Christensen, MJ (1996) Antifungal activity in grasses infected with Acremonium and Epichloë endophytes. Australasian Plant Pathology 25, 186191.Google Scholar
Clements, DR et al. (1996) Tillage effects on weed seed return and seedbank composition. Weed Science 44, 314322.Google Scholar
Cochrane, MP (1994) Observations on the germ aleurone of barley. Phenol oxidase and peroxidase activity. Annals of Botany 73, 121128.Google Scholar
Cochrane, MP, Paterson, L and Gould, E (2000) Changes in chalazal cell walls and in the peroxidase enzymes of the crease region during grain development in barley. Journal of Experimental Botany 51, 507520.Google Scholar
Collins, T, Gerday, C and Feller, G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiology Reviews 29, 323.Google Scholar
Constabel, CP and Barbehenn, R (2008) Defensive roles of polyphenol oxidase in plants. In Schaller, A (ed), Induced Plant Resistance to Herbivory. Dordrecht: Springer Science and Business Media B.V, pp. 253270.Google Scholar
Cosio, C and Dunand, C (2008) Specific functions of individual class III peroxidase genes. Journal of Experimental Botany 60, 391408.Google Scholar
Dahiya, N, Tewari, R and Hoondal, GS (2006) Biotechnological aspects of chitinolytic enzymes: a review. Applied Microbiology and Biotechnology 71, 773782.Google Scholar
Dalling, JW et al. (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology 99, 8995.Google Scholar
Damon, C et al. (2012) Metatranscriptomics reveals the diversity of genes expressed by eukaryotes in forest soils. PloS One 7, p.e28967.Google Scholar
da Rosa-Garzon, NG et al. (2017) Medium pH in submerged cultivation modulates differences in the intracellular protein profile of Fusarium oxysporum. Preparative Biochemistry and Biotechnology 47, 664672.Google Scholar
Davidson, RM et al. (2009) Germins: a diverse protein family important for crop improvement. Plant Science 177, 499510.Google Scholar
Davis, AS et al. (2008) Chemical and physical defense of weed seeds in relation to soil seedbank persistence. Weed Science 56, 676684.Google Scholar
Davis, AS et al. (2016) Interspecific variation in persistence of buried weed seeds follows trade-offs among physiological, chemical, and physical seed defenses. Ecology and Evolution 6, 68366845.Google Scholar
de Lange, WJ and van Wilgen, BW (2010) An economic assessment of the contribution of biological control to the management of invasive alien plants and to the protection of ecosystem services in South Africa. Biological Invasions 12, 41134124.Google Scholar
de Luna, LZ et al. (2011) Mycobiota on wild oat (Avena fatua L.) seed and their caryopsis decay potential. Plant Health Progress 10, 18.Google Scholar
Delgado-Sánchez, P et al. (2011) Are fungi important for breaking seed dormancy in desert species? Experimental evidence in Opuntia streptacantha (Cactaceae). Plant Biology 13, 154159.Google Scholar
Deng, S et al. (2013) Bench scale and microplate format assay of soil enzyme activities using spectroscopic and fluorometric approaches. Applied Soil Ecology 64, 8490.Google Scholar
Deng, S et al. (2017) Comparison and standardization of soil enzyme assay for meaningful data interpretation. Journal of Microbiological Methods 133, 3234.Google Scholar
Domínguez, F and Cejudo, FJ (2014) Programmed cell death (PCD): an essential process of cereal seed development and germination. Frontiers in Plant Science 5, 366.Google Scholar
Donaldson, PA et al. (2001) Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum. Physiological and Molecular Plant Pathology 59, 297307.Google Scholar
Dong, X et al. (2008) Expressing a gene encoding wheat oxalate oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica napus). Planta 228, 331340.Google Scholar
Dong, K et al. (2012) Albumin and globulin dynamics during grain development of elite Chinese wheat cultivar Xiaoyan 6. Journal of Cereal Science 56, 615622.Google Scholar
Dong, S et al. (2014) Effector specialization in a lineage of the Irish potato famine pathogen. Science 343, 552555.Google Scholar
Dornez, E et al. (2006a) Insight into the distribution of arabinoxylans, endoxylanases, and endoxylanase inhibitors in industrial wheat roller mill streams. Journal of Agricultural and Food Chemistry 54, 85218529.Google Scholar
Dornez, E et al. (2006b) Wheat-kernel-associated endoxylanases consist of a majority of microbial and a minority of wheat endogenous endoxylanases. Journal of Agricultural and Food Chemistry 54, 40284034.Google Scholar
Dornez, E et al. (2008) Effects of genotype, harvest year and genotype-by-harvest year interactions on arabinoxylan, endoxylanase activity and endoxylanase inhibitor levels in wheat kernels. Journal of Cereal Science 47, 180189.Google Scholar
Dornez, E et al. (2010) 2-D DIGE reveals changes in wheat xylanase inhibitor protein families due to Fusarium graminearum ΔTri5 infection and grain development. Proteomics 10, 23032319.Google Scholar
Dunaevskii, YE et al. (1995) Physiological role of protease inhibitors in plants: two groups of active inhibitors in buckwheat seed. Molecular Biology 29, 747750.Google Scholar
Dunford, HB (1999) Heme Peroxidases. New York: Wiley-VCH.Google Scholar
Dunwell, JM (1998) Cupins: a new superfamily of functionally diverse proteins that include germins and plant storage proteins. Biotechnology and Genetic Engineering Reviews 15, 132.Google Scholar
Dunwell, JM, Khuri, S and Gane, PJ (2000) Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiology and Molecular Biology Reviews 64, 153179.Google Scholar
Dunwell, JM, Purvis, A and Khuri, S (2004) Cupins: the most functionally diverse protein superfamily? Phytochemistry, 65, 717.Google Scholar
Dunwell, JM et al. (2008) Germin and germin-like proteins: evolution, structure, and function. Critical Reviews in Plant Sciences 27, 342375.Google Scholar
Duo-Chuan, L (2006) Review of fungal chitinases. Mycopathologia 161, 345360.Google Scholar
Dyachok, JV et al. (2002) Endogenous Nod-factor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiology 128, 523533.Google Scholar
Ebrahim, S, Usha, K and Singh, B (2011) Pathogenesis related (PR) proteins in plant defense mechanism. Science Against Microbial Pathogens 2, 10431054.Google Scholar
Eijsink, VG et al. (2008) Towards new enzymes for biofuels: lessons from chitinase research. Trends in Biotechnology 26, 228235.Google Scholar
Elliott, GO et al. (2003) A wheat xylanase inhibitor protein (XIP-I) accumulates in the grain and has homologues in other cereals. Journal of Cereal Science 37, 187194.Google Scholar
Enkerli, J, Felix, G and Boller, T (1999) The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiology 121, 391398.Google Scholar
Fierer, N et al. (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proceedings of the National Academy of Sciences 109, 2139021395.Google Scholar
Fiers, M, Lognay, G, Fauconnier, ML and Jijakli, MH (2013) Volatile compound-mediated interactions between barley and pathogenic fungi in the soil. PLoS One 8, p.e66805.Google Scholar
Figueiredo, A, Monteiro, F and Sebastiana, M (2014) Subtilisin-like proteases in plant–pathogen recognition and immune priming: a perspective. Frontiers in Plant Science 5.Google Scholar
Finch, H, Allen, PS and Meyer, SE (2013) Environmental factors influencing Pyrenophora semeniperda-caused seed mortality in Bromus tectorum. Seed Science Research 23, 5766.Google Scholar
Flurkey, WH and Inlow, JK (2008) Proteolytic processing of polyphenol oxidase from plants and fungi. Journal of Inorganic Biochemistry 102, 21602170.Google Scholar
Franceschi, VR and Nakata, PA (2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 4171.Google Scholar
Freire, JE et al. (2015) Mo-CBP3, an antifungal chitin-binding protein from Moringa oleifera seeds, is a member of the 2S albumin family. PLoS One 10, p.e0119871.Google Scholar
Fuerst, EP et al. (2011) Induction of polyphenol oxidase activity in dormant wild oat (Avena fatua) seeds and caryopses: a defense response to seed decay fungi. Weed Science 59, 137144.Google Scholar
Fuerst, EP et al. (2014) Polyphenol oxidase as a biochemical seed defense mechanism. Frontiers in Plant Science 5.Google Scholar
Fuerst, EP et al. (2018) Induction of defense enzymes in wild oat and wheat caryopses incubated with a seed decay pathogen. Frontiers in Plant Science.Google Scholar
Fujita, K et al. (2006) A chitinase structurally related to the glycoside hydrolase family 48 is indispensable for the hormonally induced diapause termination in a beetle. Biochemical and Biophysical Research Communications 345, 502507.Google Scholar
Fujita, S et al. (1995) Purification and properties of polyphenol oxidase from cabbage (Brassica oleracea L.). Journal of Agricultural and Food Chemistry 43, 11381142.Google Scholar
Funkhouser, JD and Aronson, NN (2007) Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evolutionary Biology 7, 96.Google Scholar
Gallagher, RS et al. (2010) Phenolic and short-chained aliphatic organic acid constituents of wild oat (Avena fatua L.) seeds. Journal of Agricultural and Food Chemistry 58, 218225.Google Scholar
Gallandt, ER (2006) How can we target the weed seedbank? Weed Science 54, 588596.Google Scholar
Gallandt, ER, Fuerst, EP and Kennedy, AC (2004) Effect of tillage, fungicide seed treatment, and soil fumigation on seed bank dynamics of wild oat (Avena fatua). Weed Science 52, 597604.Google Scholar
Gao, Q et al. (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genetics 7, p.e1001264.Google Scholar
Gebruers, K et al. (2002) Endoxylanase inhibition activity in different European wheat cultivars and milling fractions. Cereal Chemistry 79, 613616.Google Scholar
Gebruers, K et al. (2010) Variability in xylanase and xylanase inhibition activities in different cereals in the HEALTHGRAIN diversity screen and contribution of environment and genotype to this variability in common wheat. Journal of Agricultural and Food Chemistry 58, 93629371.Google Scholar
Godwin, J, Raviv, B and 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 6, 64.Google Scholar
Gerdemann, C et al. (2002a) Comparative modeling of the latent form of a plant catechol oxidase using a molluskan hemocyanin structure. Journal of Inorganic Biochemistry 89, 155158.Google Scholar
Gerdemann, C, Eicken, C and Krebs, B (2002b) The crystal structure of catechol oxidase: new insight into the function of type-3 copper proteins. Accounts of Chemical Research 35, 183191.Google Scholar
German, DP et al. (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology and Biochemistry 43, 13871397.Google Scholar
Gianessi, LP and Reigner, NP (2007) The value of herbicides in US crop production. Weed Technology 21, 559566.Google Scholar
Giardina, P et al. (2010) Laccases: a never-ending story. Cellular and Molecular Life Sciences 67, 369385.Google Scholar
Gibson, DJ, Young, BG and Wood, AJ (2017) Can weeds enhance profitability? Integrating ecological concepts to address crop–weed competition and yield quality. Journal of Ecology 105, 900904.Google Scholar
Girard, V et al. (2013) Secretomes: the fungal strike force. Proteomics 13, 597608.Google Scholar
Goesaert, H et al. (2003) TAXI type endoxylanase inhibitors in different cereals. Journal of Agricultural and Food Chemistry 51, 37703775.Google Scholar
Golbeck, JH and Cammarata, KV (1981) Spinach thylakoid polyphenol oxidase Isolation, activation, and properties of the native chloroplast enzyme. Plant Physiology 67, 977984.Google Scholar
Gomes, VM, Oliveira, AEA and Xavier-Filho, J (1996) A chitinase and a β-1,3-glucanase isolated from the seeds of cowpea (Vigna unguiculata L. Walp) inhibit the growth of fungi and insect pests of the seed. Journal of the Science of Food and Agriculture 72, 8690.Google Scholar
Gomez, L et al. (2002) Seed chitinases. Seed Science Research 12, 217230.Google Scholar
Grover, A (2012) Plant chitinases: genetic diversity and physiological roles. Critical Reviews in Plant Sciences 31, 5773.Google Scholar
Güldener, U et al. (2006) Development of a Fusarium graminearum Affymetrix GeneChip for profiling fungal gene expression in vitro and in planta. Fungal Genetics and Biology 43, 316325.Google Scholar
Gys, W et al. (2004) Debranning of wheat prior to milling reduces xylanase but not xylanase inhibitor activities in wholemeal and flour. Journal of Cereal Science 39, 363369.Google Scholar
Haddad, R and Japelaghi, RH (2015) Isolation of grape peroxiredoxin gene responding to abiotic stresses. Russian Journal of Plant Physiology 62, 856865.Google Scholar
Haegi, A et al. (2008) Histological and molecular analysis of Rdg2a barley resistance to leaf stripe. Molecular Plant Pathology 9, 463478.Google Scholar
Hamid, R et al. (2013) Chitinases: an update. Journal of Pharmacy and BioAllied Sciences 5, 2129.Google Scholar
Hartl, L, Zach, S and Seidl-Seiboth, V (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Applied Microbiology and Biotechnology 93, 533543.Google Scholar
Hatsch, D et al. (2006) Fusarium graminearum on plant cell wall: no fewer than 30 xylanase genes transcribed. Biochemical and Biophysical Research Communications 345, 959966.Google Scholar
Hiraga, S et al. (2001) A large family of class III plant peroxidases. Plant and Cell Physiology 42, 462468.Google Scholar
Hofrichter, M et al. (2010) New and classic families of secreted fungal heme peroxidases. Applied Microbiology and Biotechnology 87, 871897.Google Scholar
Hong, JK and Hwang, BK (2006) Promoter activation of pepper class II basic chitinase gene, CAChi2, and enhanced bacterial disease resistance and osmotic stress tolerance in the CAChi2-overexpressing Arabidopsis. Planta 223, 433448.Google Scholar
Horn, SJ et al. (2006) Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. The FEBS Journal 273, 491503.Google Scholar
Hu, X et al. (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiology 133, 170181.Google Scholar
Hughner, RS et al. (2007) Who are organic food consumers? A compilation and review of why people purchase organic food. Journal of Consumer Behaviour 6, 94110.Google Scholar
Huynh, QK et al. (1992) Antifungal proteins from plants. Purification, molecular cloning, and antifungal properties of chitinases from maize seed. Journal of Biological Chemistry 267, 66356640.Google Scholar
Imai, K and Nakai, K (2010) Prediction of subcellular locations of proteins: where to proceed? Proteomics 10, 39703983.Google Scholar
Jackowiak, H et al. (2005) Scanning electron microscopy of Fusarium damaged kernels of spring wheat. International Journal of Food Microbiology 98, 113123.Google Scholar
Jashni, MK et al. (2015a) Synergistic action of a metalloprotease and a serine protease from Fusarium oxysporum f. sp. lycopersici cleaves chitin-binding tomato chitinases, reduces their antifungal activity, and enhances fungal virulence. Molecular Plant–Microbe Interactions 28, 9961008.Google Scholar
Jashni, MK et al. (2015b) The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant–pathogen interactions. Frontiers in Plant Science 6.Google Scholar
Jerkovic, A et al. (2010) Strategic distribution of protective proteins within bran layers of wheat protects the nutrient-rich endosperm. Plant Physiology 152, 14591470.Google Scholar
Kaintz, C, Mauracher, SG and Rompel, A (2014) Type-3 copper proteins: recent advances on polyphenol oxidases, in Christov, CZ (ed), Advances in Protein Chemistry and Structural Biology: Metal-Containing Enzymes 97, 135. San Diego, CA: Elsevier, Academic Press.Google Scholar
Kanauchi, M, Milet, J and Bamforth, CW (2009) Oxalate and oxalate oxidase in malt. Journal of the Institute of Brewing 115, 232237.Google Scholar
Karlsson, M and Stenlid, J (2008) Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evolutionary Bioinformatics 4, 4760.Google Scholar
Kasprzewska, A (2003) Plant chitinases – regulation and function. Cellular and Molecular Biology Letters 8, 809824.Google Scholar
Kastle, JH and Porch, MB (1908) The peroxidase reaction of milk. Journal of Biological Chemistry 4, 301320.Google Scholar
Kennedy, AC and Kremer, RJ (1996) Microorganisms in weed control strategies. Journal of Production Agriculture 9, 480485.Google Scholar
Kennedy, AC et al. (1991) Rhizobacteria suppressive to the weed downy brome. Soil Science Society of America Journal 55, 722727.Google Scholar
Kikot, GE, Hours, RA and Alconada, TM (2009) Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: a review. Journal of Basic Microbiology 49, 231241.Google Scholar
Kremer, RJ (1993) Management of weed seed banks with microorganisms. Ecological Applications 3, 4252.Google Scholar
Kruger, JE and LaBerge, DE (1974) Changes in peroxidase activity and peroxidase isozyme patterns of wheat during kernel growth and maturation. Cereal Chemistry 51, 345354.Google Scholar
Kubicek, CP et al. (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biology 12, R40.Google Scholar
Kudryavtseva, NN et al. (2013) Secretion of proteolytic enzymes by three phytopathogenic microorganisms. Applied Biochemistry and Microbiology 49, 514520.Google Scholar
Kumar, CG and Takagi, H (1999) Microbial alkaline proteases: from a bioindustrial viewpoint. Biotechnology Advances 17, 561594.Google Scholar
LaBerge, DE (1975) Anatomical distribution of peroxidase isozymes in barley kernels. Canadian Journal of Plant Science 55, 661666.Google Scholar
LaBerge, DE, Kruger, JE and Meredith, WOS (1973) Peroxidase isozymes in mature barley kernels. Canadian Journal of Plant Science 53, 705713.Google Scholar
Lane, BG (1994) Oxalate, germin, and the extracellular matrix of higher plants. The FASEB Journal 8, 294301.Google Scholar
Lane, BG (2000) Oxalate oxidases and differentiating surface structure in wheat: germins. Biochemical Journal 349, 309321.Google Scholar
Lane, BG (2002) Oxalate, germins, and higher-plant pathogens. IUBMB Life 53, 6775.Google Scholar
Lange, J et al. (1996) Proteolytic processing of class IV chitinase in the compatible interaction of bean roots with Fusarium solani. Plant Physiology 111, 11351144.Google Scholar
Langner, T and Göhre, V (2016) Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions. Current Genetics 62, 243254.Google Scholar
Langner, T et al. (2015) Chitinases are essential for cell separation in Ustilago maydis. Eukaryotic Cell 14, 846857.Google Scholar
Lásztity, R (1999) Cereal Chemistry. Akadémiai Kiadoó, Budapest.Google Scholar
Latgé, JP (2007) The cell wall: a carbohydrate armour for the fungal cell. Molecular Microbiology 66, 279290.Google Scholar
Leah, R et al. (1991) Biochemical and molecular characterization of three barley seed proteins with antifungal properties. Journal of Biological Chemistry 266, 15641573.Google Scholar
Lederberg, J and McCray, AT (2001) Ome sweetomics – a genealogical treasury of words. The Scientist 15, 8.Google Scholar
Li, XC et al. (2015) Divergent biochemical and enzymatic properties of oxalate oxidase isoforms encoded by four similar genes in rice. Phytochemistry 118, 216223.Google Scholar
Liebman, M and Davis, AS (2000) Integration of soil, crop and weed management in low-external-input farming systems. Weed Research-Oxford 40, 2748.Google Scholar
Livingstone, DM et al. (2005) Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene. Plant Physiology 137, 13541362.Google Scholar
Lombard, V et al. (2013) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Research 42, D490495.Google Scholar
Marcus, JP et al. (1999) A family of antimicrobial peptides is produced by processing of a 7S globulin protein in Macadamia integrifolia kernels. The Plant Journal 19, 699710.Google Scholar
Martin, MPLD and Field, RJ (1988) Influence of time of emergence of wild oat on competition with wheat. Weed Research 28, 111116.Google Scholar
Marusek, CM et al. (2006) Comparative analysis of polyphenol oxidase from plant and fungal species. Journal of Inorganic Biochemistry 100, 108123.Google Scholar
Masuda, T, Zhao, G and Mikami, B (2015) Crystal structure of class III chitinase from pomegranate provides the insight into its metal storage capacity. Bioscience, Biotechnology, and Biochemistry 79, 4550.Google Scholar
Mayer, AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67, 23182331.Google Scholar
McCleary, BV et al. (2015) Hydrolysis of wheat flour arabinoxylan, acid-debranched wheat flour arabinoxylan and arabino-xylo-oligosaccharides by β-xylanase, α-L-arabinofuranosidase and β-xylosidase. Carbohydrate Research 407, 7996.Google Scholar
Menalled, FD, Gross, KL and Hammond, M (2001) Weed aboveground and seedbank community responses to agricultural management systems. Ecological Applications 11, 15861601.Google Scholar
Metraux, JP and Boller, TH (1986) Local and systemic induction of chitinase in cucumber plants in response to viral, bacterial and fungal infections. Physiological and Molecular Plant Pathology 28, 161169.Google Scholar
Meyer, SE et al. (2007) Impact of the pathogen Pyrenophora semeniperda on Bromus tectorum seedbank dynamics in North American cold deserts. Weed Research 47, 5462.Google Scholar
Meyer, SE et al. (2008) A seed bank pathogen causes seedborne disease: Pyrenophora semeniperda on undispersed grass seeds in western North America. Canadian Journal of Plant Pathology 30, 525533.Google Scholar
Meyer, SE, Stewart, TE and Clement, S (2010) The quick and the deadly: growth vs virulence in a seed bank pathogen. New Phytologist 187, 209216.Google Scholar
Mohammadi, M and Kazemi, H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Science 162, 491498.Google Scholar
Monod, M et al. (2002) Secreted proteases from pathogenic fungi. International Journal of Medical Microbiology 292, 405419.Google Scholar
Müller-Stöver, D et al. (2016) Contribution of the seed microbiome to weed management. Weed Research 56, 335339.Google Scholar
Naumann, TA, Wicklow, DT and Kendra, DF (2009) Maize seed chitinase is modified by a protein secreted by Bipolaris zeicola. Physiological and Molecular Plant Pathology 74, 134141.Google Scholar
Naumann, TA and Wicklow, DT (2010) Allozyme-specific modification of a maize seed chitinase by a protein secreted by the fungal pathogen Stenocarpella maydis. Phytopathology 100, 645654.Google Scholar
Naumann, TA, Wicklow, DT and Price, NP (2011) Identification of a chitinase-modifying protein from Fusarium verticillioides truncation of a host resistance protein by a fungalysin metalloprotease. Journal of Biological Chemistry 286, 3535835366.Google Scholar
Nightingale, MJ et al. (1999) Fusarium head blight: effect of fungal proteases on wheat storage proteins. Cereal Chemistry 76, 150158.Google Scholar
Noda, J, Brito, N and González, C (2010) The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biology 10, 38.Google Scholar
Noots, I, Delcour, JA and Michiels, CW (1999) From field barley to malt: detection and specification of microbial activity for quality aspects. Critical Reviews in Microbiology 25, 121153.Google Scholar
Oerke, EC (2006) Crop losses to pests. The Journal of Agricultural Science 144, 3143.Google Scholar
Olivieri, F et al. (2002) Characterization of an extracellular serine protease of Fusarium eumartii and its action on pathogenesis related proteins. European Journal of Plant Pathology 108, 6372.Google Scholar
Olivieri, FP et al. (2004) Hydrolytic activities of Fusarium solani and Fusarium solani f. sp. eumartii associated with the infection process of potato tubers. Journal of Phytopathology 152, 337344.Google Scholar
Paës, G, Berrin, JG and Beaugrand, J (2012) GH11 xylanases: structure/function/properties relationships and applications. Biotechnology Advances 30, 564592.Google Scholar
Pake, CE and Venable, DL (1996) Seed banks in desert annuals: implications for persistence and coexistence in variable environments. Ecology 77, 14271435.Google Scholar
Passardi, F et al. (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65, 18791893.Google Scholar
Passardi, F et al. (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Reports 24, 255265.Google Scholar
Patil, RS, Ghormade, V and Deshpande, MV (2000) Chitinolytic enzymes: an exploration. Enzyme and Microbial Technology 26, 473483.Google Scholar
Pekkarinen, AI, Jones, BL and Niku-Paavola, ML (2002) Purification and properties of an alkaline proteinase of Fusarium culmorum. The FEBS Journal 269, 798807.Google Scholar
Pekkarinen, AI and Jones, BL (2003) Purification and identification of barley (Hordeum vulgare L.) proteins that inhibit the alkaline serine proteinases of Fusarium culmorum. Journal of Agricultural and Food Chemistry 51, 710717.Google Scholar
Pekkarinen, AI et al. (2003) Fusarium species synthesize alkaline proteinases in infested barley. Journal of Cereal Science 37, 349356.Google Scholar
Peñuelas, J et al. (2014) Biogenic volatile emissions from the soil. Plant, Cell and Environment 37, 18661891.Google Scholar
Peumans, WJ and Van Damme, EJ (1995) Lectins as plant defense proteins. Plant Physiology 109, 347352.Google Scholar
Pfeiffer, TW et al. (2003) Increased soybean pubescence density. Crop Science 43, 20712076.Google Scholar
Pimentel, D, Zuniga, R and Morrison, D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52, 273288.Google Scholar
Polizeli, MLTM et al. (2005) Xylanases from fungi: properties and industrial applications. Applied Microbiology and Biotechnology 67, 577591.Google Scholar
Pollet, A, Delcour, JA, and Courtin, CM (2010). Structural determinants of the substrate specificities of xylanases from different glycoside hydrolase families. Critical Reviews in Biotechnology 30, 176191.Google Scholar
Pourcel, L et al. (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. The Plant Cell 17, 29662980.Google Scholar
Ramos, AL et al. (1998) Distribution of defense-related enzymatic activities in the quiescent organs of Phaseolus vulgaris L. seeds. Bioscience, Biotechnology, and Biochemistry 62, 5459.Google Scholar
Rao, MB et al. (1998) Molecular and biotechnological aspects of microbial proteases. Microbiology and Molecular Biology Reviews 62, 597635.Google Scholar
Raviv, B et al. (2017a) The dead seed coat functions as a long-term storage for active hydrolytic enzymes. PloS One 12, p.e0181102.Google Scholar
Raviv, B et al. (2017b) 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, p.e0177537.Google Scholar
Rawlings, ND, Barrett, AJ and Finn, RD (2016) Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Research 44, D343350.Google Scholar
Requena, L and Bornemann, S (1999) Barley (Hordeum vulgare) oxalate oxidase is a manganese-containing enzyme. Biochemical Journal 343, 185190.Google Scholar
Robert, N et al. (2002) Expression of grapevine chitinase genes in berries and leaves infected by fungal or bacterial pathogens. Plant Science 162, 389400.Google Scholar
Rodríguez-Serrano, M et al. (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiology 150, 229243.Google Scholar
Rose, TL et al. (2006) Defense proteins from Vigna unguiculata seed exudates: characterization and inhibitory activity against Fusarium oxysporum. Plant and Soil 286, 181191.Google Scholar
Rosenthal, GA (1977) Nitrogen allocation for L-canavanine synthesis and its relationship to chemical defense of the seed. Biochemical Systematics and Ecology 5, 219220.Google Scholar
Rouhier, N et al. (2004) Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant functional in pathogen defense. Plant Physiology 134, 10271038.Google Scholar
Saleh-Lakha, S et al. (2011) Challenges in quantifying microbial gene expression in soil using quantitative reverse transcription real-time PCR. Journal of Microbiological Methods 85, 239243.Google Scholar
Sales, MP et al. (2000) Do legume storage proteins play a role in defending seeds against bruchids? Plant Physiology 124, 515522.Google Scholar
Samad, A et al. (2017) Shared and host-specific microbiome diversity and functioning of grapevine and accompanying weed plants. Environmental Microbiology 19, 14071424.Google Scholar
Santos, IS et al. (2004) A chitinase from Adenanthera pavonina L. seeds: purification, characterisation and immunolocalisation. Plant Science 167, 12031210.Google Scholar
Sauerborn, J et al. (1996) Electron microscopic analysis of the penetration process of Fusarium nygamai, a hyperparasite of Striga hermonthica. Biological Control 7, 5359.Google Scholar
Schinner, F and von Mersi, W (1990) Xylanase-, CM-cellulase- and invertase activity in soil: an improved method. Soil Biology and Biochemistry 22, 511515.Google Scholar
Schlumbaum, A et al. (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324, 365367.Google Scholar
Scialabba, N (2000) Factors influencing organic agriculture policies with a focus on developing countries. In Proceedings from the 13th IFOAM Scientific Conference, August 2000, Basel, Switzerland.Google Scholar
Seidl, V (2008) Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biology Reviews 22, 3642.Google Scholar
Seidl, V et al. (2005) A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. The FEBS Journal 272, 59235939.Google Scholar
Sella, L et al. (2013) A Fusarium graminearum xylanase expressed during wheat infection is a necrotizing factor but is not essential for virulence. Plant Physiology and Biochemistry 64, 110.Google Scholar
Sharma, KM et al. (2017) Microbial alkaline proteases: Optimization of production parameters and their properties. Journal of Genetic Engineering and Biotechnology 15, 115126.Google Scholar
Siemens, DH, Johnson, CD and Ribardo, KJ (1992) Alternative seed defense mechanisms in congeneric plants. Ecology 73, 21522166.Google Scholar
Skadhauge, B, Thomsen, KK and Wettstein, D (1997) The role of the barley testa layer and its flavonoid content in resistance to Fusarium infections. Hereditas 126, 147160.Google Scholar
Slavokhotova, AA et al. (2014) Novel mode of action of plant defense peptides–hevein-like antimicrobial peptides from wheat inhibit fungal metalloproteases. The FEBS Journal 281, 47544764.Google Scholar
Soberanes-Gutiérrez, CV et al. (2015) The pep4 gene encoding proteinase A is involved in dimorphism and pathogenesis of Ustilago maydis. Molecular Plant Pathology 16, 837846.Google Scholar
Soltani, N et al. (2016) Potential corn yield losses from weeds in North America. Weed Technology 30, 979984.Google Scholar
Soltani, N et al. (2017) Perspectives on potential soybean yield losses from weeds in North America. Weed Technology 31, 148154.Google Scholar
Sreenivasulu, N et al. (2006) Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA-regulated maturation in developing barley seeds. The Plant Journal 47, 310327.Google Scholar
Staats, CC et al. (2013) Fungal zinc metabolism and its connections to virulence. Frontiers in Cellular and Infection Microbiology, 3.Google Scholar
Stacy, RA et al. (1996) A peroxiredoxin antioxidant is encoded by a dormancy-related gene, Per1, expressed during late development in the aleurone and embryo of barley grains. Plant Molecular Biology 31, 12051216.Google Scholar
Steinweg, JM, Dukes, JS and Wallenstein, MD (2012) Modeling the effects of temperature and moisture on soil enzyme activity: linking laboratory assays to continuous field data. Soil Biology and Biochemistry 55, 8592.Google Scholar
Su, Y et al. (2014) ScChi, encoding an acidic class III chitinase of sugarcane, confers positive responses to biotic and abiotic stresses in sugarcane. International Journal of Molecular Sciences 15, 27382760.Google Scholar
Sultan, A et al. (2016) Exploring the plant–microbe interface by profiling the surface-associated proteins of barley grains. Journal of Proteome Research 15, 11511167.Google Scholar
Swanton, CJ and Weise, SF (1991) Integrated weed management: the rationale and approach. Weed Technology 5, 657663.Google Scholar
Taira, T et al. (2001) Localization, accumulation, and antifungal activity of chitinases in rye (Secale cereale) seed. Bioscience, Biotechnology, and Biochemistry 65, 27102718.Google Scholar
Terras, FR et al. (1992) Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. Journal of Biological Chemistry 267, 1530115309.Google Scholar
Terras, FR et al. (1993) A new family of basic cysteine-rich plant antifungal proteins from Brassicaceae species. FEBS Letters 316, 233240.Google Scholar
Thompson, EW and Lane, BG (1980) Relation of protein synthesis in imbibing wheat embryos to the cell-free translational capacities of bulk mRNA from dry and imbibing embryos. Journal of Biological Chemistry 255, 59655970.Google Scholar
Thompson, K and Grime, JP (1979) Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. The Journal of Ecology 67, 893921.Google Scholar
Tran, LT and Constabel, CP (2011) The polyphenol oxidase gene family in poplar: phylogeny, differential expression and identification of a novel, vacuolar isoform. Planta 234, 799813.Google Scholar
Trümper, C et al. (2016) Identification of regulated proteins in naked barley grains (Hordeum vulgare nudum) after Fusarium graminearum infection at different grain ripening stages. Journal of Proteomics 133, 8692.Google Scholar
Upchurch, RG and Ramirez, ME (2010) Defense-related gene expression in soybean leaves and seeds inoculated with Cercospora kikuchii and Diaporthe phaseolorum var. meridionalis. Physiological and Molecular Plant Pathology 75, 6470.Google Scholar
Vámos-Vigyázó, L and Haard, NF (1981) Polyphenol oxidases and peroxidases in fruits and vegetables. Critical Reviews in Food Science and Nutrition 15, 49127.Google Scholar
van den Brink, J and de Vries, RP (2011) Fungal enzyme sets for plant polysaccharide degradation. Applied Microbiology and Biotechnology 91, 14771492.Google Scholar
van Gelder, CW, Flurkey, WH and Wichers, HJ (1997) Sequence and structural features of plant and fungal tyrosinases. Phytochemistry 45, 13091323.Google Scholar
van Hengel, AJ et al. (2001) N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiology 125, 18801890.Google Scholar
van Hengel, AJ, Van Kammen, AB and De Vries, SC (2002) A relationship between seed development, arabinogalactan-proteins (AGPs) and the AGP mediated promotion of somatic embryogenesis. Physiologia Plantarum 114, 637644.Google Scholar
Wagner, NC et al. (2007) Developing an empirical yield-prediction model based on wheat and wild oat (Avena fatua) density, nitrogen and herbicide rate, and growing-season precipitation. Weed Science 55, 652664.Google Scholar
Wagner, M and Mitschunas, N (2008) Fungal effects on seed bank persistence and potential applications in weed biocontrol: a review. Basic and Applied Ecology 9, 191203.Google Scholar
Walker, JR and Ferrar, PH (1998) Diphenol oxidases, enzyme-catalysed browning and plant disease resistance. Biotechnology and Genetic Engineering Reviews 15, 457498.Google Scholar
Wallenstein, MD and Weintraub, MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biology and Biochemistry 40, 20982106.Google Scholar
Wang, T et al. (2010) Identification of seed proteins associated with resistance to pre-harvested aflatoxin contamination in peanut (Arachis hypogaea L). BMC Plant Biology 10, 267.Google Scholar
Warnock, DW (1971) Assay of fungal mycelium in grains of barley, including the use of the fluorescent antibody technique for individual fungal species. Microbiology 67, 197205.Google Scholar
Welinder, KG (1985) Plant peroxidases. The FEBS Journal 151, 497504.Google Scholar
Welinder, KG (1992) Superfamily of plant, fungal and bacterial peroxidases. Current Opinion in Structural Biology 2, 388393.Google Scholar
Wilson, JS and Otsuki, T (2004) To spray or not to spray: pesticides, banana exports, and food safety. Food Policy 29, 131146.Google Scholar
Wong, KK, Tan, LU and Saddler, JN (1988) Multiplicity of beta-1,4-xylanase in microorganisms: functions and applications. Microbiological Reviews 52, 305317.Google Scholar
Woo, EJ et al. (1998) Barley oxalate oxidase is a hexameric protein related to seed storage proteins: evidence from X-ray crystallography. FEBS Letters 437, 8790.Google Scholar
Woo, EJ et al. (2000) Germin is a manganese containing homohexamer with oxalate oxidase and superoxide dismutase activities. Nature Structural and Molecular Biology 7, 10361040.Google Scholar
Wu, S et al. (2000) Functional characterization of seed coat-specific members of the barley germin gene family. Plant Physiology and Biochemistry 38, 685698.Google Scholar
Ye, XY and Ng, TB (2002) Isolation of a novel peroxidase from French bean legumes and first demonstration of antifungal activity of a non-milk peroxidase. Life Sciences 71, 16671680.Google Scholar
Yeboah, NA et al. (1998) A class III acidic endochitinase is specifically expressed in the developing seeds of soybean (Glycine max [L.] Merr.). Plant Molecular Biology 36, 407415.Google Scholar
Yike, I (2011) Fungal proteases and their pathophysiological effects. Mycopathologia 171, 299323.Google Scholar
Yoruk, R and Marshall, MR (2003) Physicochemical properties and function of plant polyphenol oxidase: a review. Journal of Food Biochemistry 27, 361422.Google Scholar
Zekiri, F et al. (2014) Purification and characterization of tyrosinase from walnut leaves (Juglans regia). Phytochemistry 101, 515.Google Scholar
Zhao, Z et al. (2013) Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14, 274.Google Scholar
Zhu, Q et al. (1994) Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Nature Biotechnology 12, 807812.Google Scholar
Zimdahl, RL (1988) The concept and application of the critical weed-free period. In Altieri, MA and Liebman, M (eds), Weed Management in Agroecosystems: Ecological Approaches. Boca Raton, FL: CRC Press, pp. 145155.Google Scholar
Zimmermann, G et al. (2006) The multigene family encoding germin-like proteins of barley. Regulation and function in basal host resistance. Plant Physiology 142, 181192.Google Scholar