Arabinogalactan Protein-Like Proteins From Ulva lactuca Activate Immune Responses and Plant Resistance in an Oilseed Crop

. 2022 ; 13 () : 893858. [epub] 20220520

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35668790

Natural compounds isolated from macroalgae are promising, ecofriendly, and multifunctional bioinoculants, which have been tested and used in agriculture. Ulvans, for instance, one of the major polysaccharides present in Ulva spp. cell walls, have been tested for their plant growth-promoting properties as well as their ability to activate plant immune defense, on a large variety of crops. Recently, we have characterized for the first time an arabinogalactan protein-like (AGP-like) from Ulva lactuca, which exhibits several features associated to land plant AGPs. In land plant, AGPs were shown to play a role in several plant biological functions, including cell morphogenesis, reproduction, and plant-microbe interactions. Thus, isolated AGP-like proteins may be good candidates for either the plant growth-promoting properties or the activation of plant immune defense. Here, we have isolated an AGP-like enriched fraction from Ulva lactuca and we have evaluated its ability to (i) protect oilseed rape (Brassica napus) cotyledons against Leptosphaeria maculans, and (ii) its ability to activate immune responses. Preventive application of the Ulva AGP-like enriched fraction on oilseed rape, followed by cotyledon inoculation with the fungal hemibiotroph L. maculans, resulted in a major reduction of infection propagation. The noticed reduction correlated with an accumulation of H2O2 in treated cotyledons and with the activation of SA and ET signaling pathways in oilseed rape cotyledons. In parallel, an ulvan was also isolated from Ulva lactuca. Preventive application of ulvan also enhanced plant resistance against L. maculans. Surprisingly, reduction of infection severity was only observed at high concentration of ulvan. Here, no such significant changes in gene expression and H2O2 production were observed. Together, this study indicates that U. lactuca AGP-like glycoproteins exhibit promising elicitor activity and that plant eliciting properties of Ulva extract, might result not only from an ulvan-originated eliciting activities, but also AGP-like originated.

Zobrazit více v PubMed

Abouraïcha E., El Alaoui-Talibi Z., El Boutachfaiti R., Petit E., Courtois B., Courtois J., et al. . (2015). Induction of natural defense and protection against Penicillium expansum and Botrytis cinerea in apple fruit in response to bioelicitors isolated from green algae. Sci. Hortic. 181, 121–128. doi: 10.1016/j.scienta.2014.11.002 DOI

Ali O., Ramsubhag A., Jayaraman J. (2021). Biostimulant properties of seaweed extracts in plants, implications towards sustainable crop production. Plan. Theory 10:531. doi: 10.3390/plants10030531, PMID: PubMed DOI PMC

Allègre M., Héloir M.-C., Trouvelot S., Daire X., Pugin A., Wendehenne D., et al. . (2009). Are grapevine stomata involved in the elicitor-induced protection against downy mildew? MPMI 22, 977–986. doi: 10.1094/MPMI-22-8-0977, PMID: PubMed DOI

Aquino R. S., Grativol C., Mourão P. A. S. (2011). Rising from the sea, correlations between sulfated polysaccharides and salinity in plants. PLoS One 6:e18862. doi: 10.1371/journal.pone.0018862, PMID: PubMed DOI PMC

Aziz A., Poinssot B., Daire X., Adrian M., Bézier A., Lambert B., et al. . (2003). Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmospara viticola. MPMI 16, 1118–1128. doi: 10.1094/MPMI.2003.16.12.1118, PMID: PubMed DOI

Balesdent M. H., Attard A., Ansan-Melayah D., Delourme R., Renard M., Rouxel T. (2001). Genetic control and host range of avirulence toward Brassica napus cultivars Quinta and jet Neuf in Leptosphaeria maculans. Phytopathology 91, 70–76. doi: 10.1094/PHYTO.2001.91.1.70, PMID: PubMed DOI

Barna B., Fodor J., Harrach B. D., Pogány M., Király Z. (2012). The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol. Biochem. 59, 37–43. doi: 10.1016/j.plaphy.2012.01.014, PMID: PubMed DOI

Bartels D., Baumann A., Maeder M., Geske T., Heise E. M., von Schwartzenberg K., et al. . (2017). Evolution of plant cell wall: arabinogalactan-proteins from three moss genera show structural differences compared to seed plants. Carbohydr. Polym. 163, 227–235. doi: 10.1016/j.carbpol.2017.01.043, PMID: PubMed DOI

Bartels D., Classen B. (2017). Structural investigations on arabinogalactan-proteins from a lycophyte and different monilophytes (ferns) in the evolutionary context. Carbohydr. Polym. 172, 342–351. doi: 10.1016/j.carbpol.2017.05.031, PMID: PubMed DOI

Battacharyya D., Babgohari M. Z., Rathor P., Prithiviraj B. (2015). Seaweed extracts as biostimulants in horticulture. Sci. Hortic. 196, 39–48. doi: 10.1016/j.scienta.2015.09.012, PMID: PubMed DOI

Becker M. G., Zhang X., Walker P. L., Wan J. C., Millar J. L., Khan D., et al. . (2017). Transcriptome analysis of the Brassica napus–Leptosphaeria maculans pathosystem identifies receptor, signaling and structural genes underlying plant resistance. Plant J. 90, 573–586. doi: 10.1111/tpj.13514, PMID: PubMed DOI

Benedetti M., Pontiggia D., Raggia S., Cheng Z., Scalonia F., Ferrari S., et al. . (2015). Plant immunity triggered by engineered in vivo releaseof oligogalacturonides, damage-associated molecular patterns. PNAS 112, 5533–5538. doi: 10.1073/pnas.1504154112, PMID: PubMed DOI PMC

Bigeard J., Colcombet J., Hirt H. (2015). Signaling mechanisms in pattern-triggered immunity (PTI). Mol. Plant 8, 521–539. doi: 10.1016/j.molp.2014.12.022, PMID: PubMed DOI

Blumenkrantz N., Asboe-Hansen G. (1973). New method for quantitative determination of uronic acids. Anal. Biochem. 54, 484–489. doi: 10.1016/0003-2697(73)90377-1, PMID: PubMed DOI

Boller T., Felix G. (2009). A renaissance of elicitors, perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379–406. doi: 10.1146/annurev.arplant.57.032905.105346, PMID: PubMed DOI

Bollig K., Lamshöft M., Schweimer K., Marner F.-J., Budzikiewicz H., Waffenschmidt S. (2007). Structural analysis of linear hydroxyproline-bound O-glycans of Chlamydomonas reinhardtii—conservation of the inner core in Chlamydomonas and land plants. Carbohydr. Res. 342, 2557–2566. doi: 10.1016/j.carres.2007.08.008, PMID: PubMed DOI

Borba M. C., Stadnik M. B., Stadnik M. J. (2019). Ulvan enhances seedling emergence and reduces Fusarium wilt severity in common bean (Phaseolus vulgaris L.). Crop Prot. 118, 66–71. doi: 10.1016/j.cropro.2018.12.014 DOI

Borba M. C., Velho A. C., Maia-Grondard A., Baltenweck R., Magnin-Robert M., Randoux B., et al. . (2021). The algal polysaccharide Ulvan induces resistance in wheat against Zymoseptoria tritici without major alteration of leaf Metabolome. Front. Plant Sci. 12:703712. doi: 10.3389/fpls.2021.703712, PMID: PubMed DOI PMC

Bürger M., Chory J. (2019). Stressed out about hormones, how plants orchestrate immunity. Cell Host Microbe 26, 163–172. doi: 10.1016/j.chom.2019.07.006, PMID: PubMed DOI PMC

Burketova L., Trda L., Ott P. G., Valentova O. (2015). Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol. Adv. 33, 994–1004. doi: 10.1016/j.biotechadv.2015.01.004, PMID: PubMed DOI

Capek P., Matulová M., Combourieu B. (2008). The extracellular proteoglycan produced by Rhodella grisea. Int. J. Biol. Macromol. 43, 390–393. doi: 10.1016/j.ijbiomac.2008.07.015, PMID: PubMed DOI

Carvalho F. P. (2006). Agriculture, pesticides, food security and food safety. Environ. Sci. Pol. 9, 685–692. doi: 10.1016/j.envsci.2006.08.002, PMID: PubMed DOI

Castellanos-Barriga L. G., Santacruz-Ruvalcaba F., Hernández-Carmona G., Ramírez-Briones E., Hernández-Herrera R. M. (2017). Effect of seaweed liquid extracts from Ulva lactuca on seedling growth of mung bean (Vigna radiata). J. Appl. Phycol. 29, 2479–2488. doi: 10.1007/s10811-017-1082-x DOI

Chapman J. M., Muhlemann J. K., Gayomba S. R., Muday G. K. (2019). RBOH-dependent ROS synthesis and ROS scavenging by plant specialized metabolites to modulate plant development and stress responses. Chem. Res. Toxicol. 32, 370–396. doi: 10.1021/acs.chemrestox.9b00028, PMID: PubMed DOI PMC

Chbani A., Majed S., Mawlawi H. (2015). Mineral content of mediterranean seaweeds, Padina pavonica L. (Pheophytae), Ulva lactuca L. and Ulva linza L. (Chlorophytae) for biofertilizing use. Int. J. Hortic. Sci. Technol. 2, 133–140. doi: 10.22059/IJHST.2015.56430 DOI

Chen Q., Chen Z., Lu L., Jin H., Sun L., Yu Q., et al. . (2013). Interaction between abscisic acid and nitric oxide in PB90-induced catharanthine biosynthesis of catharanthus roseus cell suspension cultures. Biotechnol. Prog. 29, 994–1001. doi: 10.1002/btpr.1738, PMID: PubMed DOI

Cluzet S., Torregrosa C., Jacquet C., Lafitte C., Fournier J., Mercier L., et al. . (2004). Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva spp. Plant Cell Environ. 27, 917–928. doi: 10.1111/j.1365-3040.2004.01197.x DOI

Cook J., Zhang J., Norrie J., Blal B., Cheng Z. (2018). Seaweed extract (Stella Maris®) activates innate immune responses in Arabidopsis thaliana and protects host against bacterial pathogens. Mar. Drugs 16:221. doi: 10.3390/md16070221, PMID: PubMed DOI PMC

Cramer G. R., Läuchli A., Polito V. S. (1985). Displacement of Ca2+ by Na+ from the plasmalemma of root cells. Plant Physiol. 79, 207–211. doi: 10.1104/pp.79.1.207, PMID: PubMed DOI PMC

Divya K., Roja N., Padal S. B. (2015). Influence of seaweed liquid fertilizer of Ulva lactuca on the seed germination, growth, productivity of Abelmoschus esculentus (L.). Int. J. Pharmacol. Res. 5, 344–356.

Dominguez H., Loret E. P. (2019). Ulva lactuca, a source of troubles and potential riches. Mar. Drugs 17:357. doi: 10.3390/md17060357, PMID: PubMed DOI PMC

Domozych D., Ciancia M., Fangel J. U., Mikkelsen M. D., Ulvskov P., Willats W. G. T. (2012). The cell walls of green algae, a journey through evolution and diversity. Front. Plant Sci. 3:82. doi: 10.3389/fpls.2012.00082, PMID: PubMed DOI PMC

Domozych D. S., Elliott L., Kiemle S. N., Gretz M. R. (2007). Pleurotaenium trabecula, a desmid of wetland biofilms: the extracellular matrix and adhesion mechanisms. J. Phycol. 43, 1022–1038. doi: 10.1111/j.1529-8817.2007.00389.x DOI

Domozych D. S., Sørensen I., Pettolino F. A., Bacic A., Willats W. G. T. (2010). The cell wall polymers of the charophycean green alga Chara corallina: immunobinding and biochemical screening. Int. J. Plant Sci. 171, 345–361. doi: 10.1086/651227 DOI

Domozych D. S., Wilson R., Domozych C. R. (2009). Photosynthetic eukaryotes of freshwater wetland biofilms: adaptations and structural characteristics of the extracellular matrix in the green alga, Cosmarium reniforme (Zygnematophyceae, Streptophyta). J. Eukaryot. Microbiol. 56, 314–322. doi: 10.1111/j.1550-7408.2009.00392.x, PMID: PubMed DOI

du Jardin P., Xu L., Geelen D. (2020). “Agricultural functions and action mechanisms of plant biostimulants (PBs)” in The Chemical Biology of Plant Biostimulants. eds. Geelen D., Xu L. (Chichester, UK: John Wiley, and Sons, Ltd.), 1–30.

Eder M., Tenhaken R., Driouich A., Lütz-Meindl U. (2008). Occurrence and characterization of arabinogalactan-like proteins and hemicelluloses in Micrasterias (Streptophyta). J. Phycol. 44, 1221–1234. doi: 10.1111/j.1529-8817.2008.00576.x, PMID: PubMed DOI

El Boukhari M. E. M., Barakate M., Bouhia Y., Lyamlouli K. (2020). Trends in seaweed extract based biostimulants, manufacturing process and beneficial effect on soil-plant systems. Plan. Theory 9:359. doi: 10.3390/plants9030359, PMID: PubMed DOI PMC

Estevez J. M., Fernández P. V., Kasulin L., Dupree P., Ciancia M. (2009). Chemical and in situ characterization of macromolecular components of the cell walls from the green seaweed Codium fragile. Glycobiology 19, 212–228. doi: 10.1093/glycob/cwn101, PMID: PubMed DOI

Estevez J. M., Leonardi P. I., Alberghina J. S. (2008). Cell wall carbohydrate epitopes in the green alga Oedogonium Bharuchae F. Minor (Oedogoniales, Chlorophyta)1. J. Phycol. 44, 1257–1268. doi: 10.1111/j.1529-8817.2008.00568.x, PMID: PubMed DOI

Fernández P. V., Ciancia M., Miravalles A. B., Estevez J. M. (2010). Cell-wall polymer mapping in the coenocytic macroalga Codium Vermilara (Bryopsidales, Chlorophyta). J. Phycol. 46, 456–465. doi: 10.1111/j.1529-8817.2010.00821.x DOI

Fernández P. V., Raffo M. P., Alberghina J., Ciancia M. (2015). Polysaccharides from the green seaweed Codium decorticatum. Structure and cell wall distribution. Carbohydr. Polym. 117, 836–844. doi: 10.1016/j.carbpol.2014.10.039, PMID: PubMed DOI

Freitas M. B., Stadnik M. J. (2012). Race-specific and ulvan-induced defense responses in bean (Phaseolus vulgaris) against Colletotrichum lindemuthianum. Physiol. Mol. Plant Pathol. 78, 8–13. doi: 10.1016/j.pmpp.2011.12.004 DOI

Freitas M. B., Stadnik M. J. (2015). Ulvan-induced resistance in Arabidopsis thaliana against Alternaria brassicicola requires reactive oxygen species derived from NADPH oxidase. Physiol. Mol. Plant Pathol. 90, 49–56. doi: 10.1016/j.pmpp.2015.03.002 DOI

Gireesh R., Haridevi C. K., Salikutty J. (2011). Effect of Ulva lactuca extract on growth and proximate composition of Vigna unguiculata (L.) Walp. J. Res. Biol. 8, 624–630.

Hahn M. G., Darvill A. G., Albersheim P. (1981). Host-pathogen interactions, XIX. The endogenous elicitor, a fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol. 68, 1161–1169. doi: 10.1104/pp.68.5.1161, PMID: PubMed DOI PMC

Hahn T., Schulz M., Stadtmüller R., Zayed A., Muffler K., Lang S., et al. . (2016). Cationic dye for the specific determination of sulfated polysaccharides. Anal. Lett. 49, 1948–1962. doi: 10.1080/00032719.2015.1126839, PMID: PubMed DOI

Happ K., Classen B. (2019). Arabinogalactan-proteins from the liverwort Marchantia polymorpha L., a member of a basal land plant lineage, are structurally different to those of angiosperms. Plan. Theory 8:460. doi: 10.3390/plants8110460, PMID: PubMed DOI PMC

Hardy M. R., Townsend R. R., Leeab Y. C. (1988). Monosaccharide analysis of glycoconjugates by anion exchange chromatography with pulsed amperometric detection. Anal. Biochem. 170, 54–62. doi: 10.1016/0003-2697(88)90089-9, PMID: PubMed DOI

Hernández-Herrera R. M., Santacruz-Ruvalcaba F., Ruiz-López M. A., Norrie J., Hernández-Carmona G. (2014). Effect of liquid seaweed extracts on growth of tomato seedlings (Solanum lycopersicum L.). J. Appl. Phycol. 26, 619–628. doi: 10.1007/s10811-013-0078-4, PMID: PubMed DOI

Hernández-Herrera R. M., Santacruz-Ruvalcaba F., Zañudo-Hernández J., Hernández-Carmona G. (2016). Activity of seaweed extracts and polysaccharide-enriched extracts from Ulva lactuca and Padina gymnospora as growth promoters of tomato and mung bean plants. J. Appl. Phycol. 28, 2549–2560. doi: 10.1007/s10811-015-0781-4 DOI

Hervé C., Siméon A., Jam M., Cassin A., Johnson K. L., Salmeán A. A., et al. . (2015). Arabinogalactan proteins have deep roots in eukaryotes, identification of genes and epitopes in brown algae and their role in Fucus serratus embryo development. New Phytol. 209, 1428–1441. doi: 10.1111/nph.13786 PubMed DOI

Huang H., Ullah F., Zhou D.-X., Yi M., Zhao Y. (2019). Mechanisms of ROS regulation of plant development and stress responses. Front. Plant Sci. 10:800. doi: 10.3389/fpls.2019.00800, PMID: PubMed DOI PMC

Jamiolkowska A. (2020). Natural compounds as elicitors of plant resistance against diseases and new biocontrol strategies. Agronomy 10:173. doi: 10.3390/agronomy100(2017)3 DOI

Jasso-Robles F. I., Gonzalez M. E., Pieckenstain F. L., Ramírez-García J. M., Guerrero-González M., Jiménez-Bremont J. F., et al. . (2020). Decrease of Arabidopsis PAO activity entails increased RBOH activity, ROS content and altered responses to pseudomonas. Plant Sci. 292:110372. doi: 10.1016/j.plantsci.2019.110372, PMID: PubMed DOI

Jaulneau V., Lafitte C., Corio-Costet M.-F., Stadnik M. J., Salamagne S., Briand X., et al. . (2011). An Ulva armoricana extract protects plants against three powdery mildew pathogens. Eur. J. Plant Pathol. 131, 393–401. doi: 10.1007/s10658-011-9816-0 DOI

Jaulneau V., Lafitte C., Jacquet C., Fournier S., Salamagne S., Briand X., et al. . (2010). Ulvan, a sulfated polysaccharide from green algae, activates plant immunity through the jasmonic acid signaling pathway. J. Biomed. Biotechnol. 2010:525291. doi: 10.1155/2010/525291, PMID: PubMed DOI PMC

Jindřichová B., Burketová L., Novotná Z. (2014). Novel properties of antimicrobial peptide anoplin. Biochem. Biophys. Res. Commun. 444, 520–524. doi: 10.1016/j.bbrc.2014.01.097, PMID: PubMed DOI

Jindřichová B., Fodor J., Šindelářová M., Burketová L., Valentová O. (2011). Role of hydrogen peroxide and antioxidant enzymes in the interaction between a hemibiotrophic fungal pathogen, Leptosphaeria maculans, and oilseed rape. Environ. Exp. Bot. 72, 149–156. doi: 10.1016/j.envexpbot.2011.02.018 DOI

Jones J. D. G., Dangl J. L. (2006). The plant immune system. Nature 444, 323–329. doi: 10.1038/nature05286, PMID: PubMed DOI

Kámán-Tóth E., Dankó T., Gullner G., Bozsó Z., Palkovics L., Pogány M. (2019). Contribution of cell wall peroxidase- and NADPH oxidase-derived reactive oxygen species to Alternaria brassicicola-induced oxidative burst in Arabidopsis. Mol. Plant Pathol. 20, 485–499. doi: 10.1111/mpp.12769, PMID: PubMed DOI PMC

Kidgell J. T., Magnusson M., de Nys R., Glasson C. R. K. (2019). Ulvan, a systematic review of extraction, composition and function. Algal Res. 39:101422. doi: 10.1016/j.algal.2019.101422 DOI

Kim P. D., Šašek V., Burketová L., Čopíková J., Synytsya A., Jindřichová B., et al. . (2013). Cell Wall components of Leptosphaeria maculans enhance resistance of Brassica napus. J. Agric. Food Chem. 61, 5207–5214. doi: 10.1021/jf401221v, PMID: PubMed DOI

Klarzynski O., Plesse B., Joubert J.-M., Yvin J.-C., Kopp M., Kloareg B., et al. . (2000). Linear b-1,3 Glucans are elicitors of defense responses in tobacco. Plant Physiol. 124, 1027–1038. doi: 10.1104/pp.124.3.1027, PMID: PubMed DOI PMC

Lahaye P. A., Epstein E. (1969). Salt toleration by plants, enhancement with calcium. Science 166, 395–396. doi: 10.1126/science.166.3903.395, PMID: PubMed DOI

Lahaye P. A., Epstein E. (1971). Calcium and salt toleration by bean plants. Physiol. Plant. 25, 213–218. doi: 10.1111/j.1399-3054.1971.tb01430.x, PMID: PubMed DOI

Lahaye P. A., Robic E. (2007). Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 6, 1765–1774. doi: 10.1021/bm061185q, PMID: PubMed DOI

Lamport D. T. A., Tan L., Held M., Kieliszewski M. J. (2018). The role of the primary cell wall in plant morphogenesis. Int. J. Mol. Sci. 19:2674. doi: 10.3390/ijms19092674, PMID: PubMed DOI PMC

Lamport D. T. A., Várnai P. (2013). Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol. 197, 58–64. doi: 10.1111/nph.12005, PMID: PubMed DOI

Lamport D. T. A., Varnai P., Seal C. E. (2014). Back to the future with the AGP–Ca2+ flux capacitor. Ann. Bot. 114, 1069–1085. doi: 10.1093/aob/mcu161, PMID: PubMed DOI PMC

Lee K. J. D., Sakata Y., Mau S. L., Pettolino F., Bacic A., Quatrano R. S., et al. . (2005). Arabinogalactan proteins are required for apical cell extension in the moss Physcomitrella patens. Plant Cell 17, 3051–3065. doi: 10.1105/tpc.105.034413, PMID: PubMed DOI PMC

Levy-Ontman O., Arad S., Harvey D. J., Parsons T. B., Fairbanks A., Tekoah Y. (2011). Unique N-glycan moieties of the 66-kDa cell wall glycoprotein from the red microalga Porphyridium sp. J. Biol. Chem. 286, 21340–21352. doi: 10.1074/jbc.M110.175042, PMID: PubMed DOI PMC

Lin Z., Lin Z., Li H., Shen S. (2012). Sequences analysis of ITS region and 18S rDNA of Ulva. ISRN Bot. 2012:468193. doi: 10.5402/2012/468193 DOI

Lipková N., Medo J., Artimová R., Maková J., Petrová J., Javoreková S., et al. . (2021). Growth promotion of rapeseed (Brassica napus L.) and blackleg disease (Leptosphaeria maculans) suppression mediated by Endophytic bacteria. Agronomy 11:1966. doi: 10.3390/agronomy11101966 DOI

Lopez-Hernandez F., Tryfona T., Rizza A., Yu X. L., Harris M. O. B., Webb A. A. R., et al. . (2020). Calcium binding by Arabinogalactan polysaccharides is important for normal plant development. Plant Cell 32, 3346–3369. doi: 10.1105/tpc.20.00027, PMID: PubMed DOI PMC

Ma Y., Yan C., Li H., Wu W., Liu Y., Wang Y., et al. . (2017). Bioinformatics prediction and evolution analysis of arabinogalactan proteins in the plant kingdom. Front. Plant Sci. 8:66. doi: 10.3389/fpls.2017.00066, PMID: PubMed DOI PMC

Ma Y., Zeng W., Bacic A., Johnson K. (2018). “AGPs through time and space” in Annual plant reviews online. ed. Roberts J. A. (Chichester, UK: John Wiley & Sons, Ltd.), 767–804.

Mareri L., Romi M., Cai G. (2019). Arabinogalactan proteins, actors or spectators during abiotic and biotic stress in plants? Plant. Biosystems 153, 173–185. doi: 10.1080/11263504.2018.1473525 DOI

Martin R. L., Le Boulch P., Clin P., Schwarzenberg A., Yvin J.-C., Andrivon D., et al. . (2020). A comparison of PTI defense profiles induced in Solanum tuberosum by PAMP and non-PAMP elicitors shows distinct, elicitor-specific responses. PLoS One 15:e0236633. doi: 10.1371/journal.pone.0236633, PMID: PubMed DOI PMC

Mathieu-Rivet E., Kiefer-Meyer M.-C., Vanier G., Ovide C., Burel C., Lerouge P., et al. . (2014). Protein N-glycosylation in eukaryotic microalgae and its impact on the production of nuclear expressed biopharmaceuticals. Front. Plant Sci. 5:359. doi: 10.3389/fpls.2014.00359, PMID: PubMed DOI PMC

Mercier L., Lafitte C., Borderies G., Briand X., Marie-Thérèse Esquerré-Tugayé M.-T., Fournier J. (2001). The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol. 149, 43–51. doi: 10.1046/j.1469-8137.2001.00011.x, PMID: PubMed DOI

Mizukami A. G., Inatsugi R., Jiao J., Kotake T., Kuwata K., Ootani K., et al. . (2016). The AMOR arabinogalactan sugar chain induces pollen-tube competency to respond to ovular guidance. Curr. Biol. 26, 1091–1097. doi: 10.1016/j.cub.2016.02.040, PMID: PubMed DOI

Mócsai R., Figl R., Troschl C., Strasser R., Svehla E., Windwarder M., et al. . (2019). N-glycans of the microalga Chlorella vulgaris are of the oligomannosidic type but highly methylated. Sci. Rep. 9:331. doi: 10.1038/s41598-018-36884-1, PMID: PubMed DOI PMC

Morales J., Kadota Y., Zipfel C., Molina A., Torres M.-A. (2016). The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. J. Exp. Bot. 67, 1663–1676. doi: 10.1093/jxb/erv558, PMID: PubMed DOI

Nabti E., Jha B., Hartmann A. (2017). Impact of seaweeds on agricultural crop production as biofertilizer. Int. J. Environ. Sci. Technol. 14, 1119–1134. doi: 10.1007/s13762-016-1202-1 DOI

Nagel A., Sirisakulwat S., Carle R., Neidhart S. (2014). An acetate−hydroxide gradient for the quantitation of the neutral sugar and Uronic acid profile of Pectins by HPAEC-PAD without Postcolumn pH adjustment. J. Agric. Food Chem. 62, 2037–2048. doi: 10.1021/jf404626d, PMID: PubMed DOI

Neik T. X., Ama J., Barbetti M., Edwards D., Batley J. (2020). Understanding host–pathogen interactions in Brassica napus in the Omics era. Plan. Theory 9:1336. doi: 10.3390/plants9101336, PMID: PubMed DOI PMC

Neik T. X., Barbetti M., Batley J. (2017). Current status and challenges in identifying disease resistance genes in Brassica napus. Front. Plant Sci. 8:1788. doi: 10.3389/fpls.2017.01788, PMID: PubMed DOI PMC

Nguema-Ona E., Coimbra S., Vicré-Gibouin M., Mollet J.-C., Driouich A. (2012). Arabinogalactan-proteins in root and pollen tube cells, distribution and functional properties. Ann. Bot. 110, 383–404. doi: 10.1093/aob/mcs143, PMID: PubMed DOI PMC

Nguema-Ona E., Vicré-Gibouin M., Cannesan M.-A., Driouich A. (2013). Arabinogalactan proteins in root–microbe interactions. Trends Plant Sci. 18, 440–449. doi: 10.1016/j.tplants.2013.03.006, PMID: PubMed DOI

Nováková M., Kim P. D., Šašek V., Burketová L., Jindřichová B., Šantrůček J., et al. . (2016). Separation and identification of candidate protein elicitors from the cultivation medium of Leptosphaeria maculans inducing resistance in Brassica napus. Biotechnol. Prog. 32, 918–928. doi: 10.1002/btpr.2266, PMID: PubMed DOI

Nováková M., Šašek V., Dobrev P. I., Valentová O., Burketová L. (2014). Plant hormones in defense response of Brassica napus to Sclerotinia sclerotiorum—reassessing the role of salicylic acid in the interaction with a necrotroph. Plant Physiol. Biochem. 80, 308–317. doi: 10.1016/j.plaphy.2014.04.019, PMID: PubMed DOI

Ogawa K., Arai M., Naganawa H., Ikeda Y., Kondo S. (2001). A new β-d-Galactan having 3-O-methyl-d-galactose from Chlorella vulgaris. J. Appl. Glycosci. 48, 325–330. doi: 10.5458/jag.48.325 DOI

Palacio-López K., Tinaz B., Holzinger A., Domozych D. S. (2019). Arabinogalactan proteins and the extracellular matrix of charophytes: a sticky business. Front. Plant Sci. 10:447. doi: 10.3389/fpls.2019.00447, PMID: PubMed DOI PMC

Paulert R., Ascrizzi R., Malatesta S., Berni P., Noseda M. D., Mazetto de Carvalho M., et al. . (2021). Ulva intestinalis extract acts as biostimulant and modulates metabolites and hormone balance in basil (Ocimum basilicum L.) and parsley (Petroselinum crispum L.). Plan. Theory 10:1391. doi: 10.3390/plants10071391, PMID: PubMed DOI PMC

Paulert R., Ebbinghaus D., Urlass C., Moerschbacher B. M. (2010). Priming of the oxidative burst in rice and wheat cell cultures by ulvan, a polysaccharide from green macroalgae, and enhanced resistance against powdery mildew in wheat and barley plants. Plant Pathol. 59, 634–642. doi: 10.1111/j.1365-3059.2010.02300.x DOI

Paulert R., Talamini V., Cassolato J. E. F., Duarte M. E. R., Noseda M. D., Smania A., et al. . (2009). Effects of sulfated polysaccharide and alcoholic extracts from green seaweed Ulva fasciata on anthracnose severity and growth of common bean (Phaseolus vulgaris L). J. Plant Dis. Prot. 116, 263–270. doi: 10.1007/BF03356321 DOI

Pfeifer L., Classen B. (2020). The cell wall of seagrasses: Fascinating, peculiar and a blank canvas for future research. Front. Plant Sci. 11:588754. doi: 10.3389/fpls.2020.588754 PubMed DOI PMC

Pfeifer L., Shafee T., Johnson K. L., Bacic A., Classen B. (2020). Arabinogalactan-proteins of Zostera marina L. contain unique glycan structures and provide insight into adaption processes to saline environments. Sci. Rep. 10:8232. doi: 10.1038/s41598-020-65135-5, PMID: PubMed DOI PMC

Pfeifer L., Utermöhlen J., Happ K., Permann C., Holzinger A., Schwartzenberg K., et al. . (2021). Search for evolutionary roots of land plant arabinogalactan-proteins in charophytes: presence of a rhamnogalactan-protein in Spirogyra pratensis (Zygnematophyceae). Plant J. 109, 568–584. doi: 10.1111/tpj.15577, PMID: PubMed DOI PMC

Přerovská T., Henka S., Bleha R., Spiwok V., Gillarová S., Yvin J.-C., et al. . (2021). Arabinogalactan-like glycoproteins from Ulva lactuca (Chlorophyta) show unique features compared to land plants AGPs. J. Phycol. 57, 619–635. doi: 10.1111/jpy.13121, PMID: PubMed DOI

Raboanatahiry N., Li H., Yu L., Li M. (2021). Rapeseed (Brassica napus), processing, utilization, and genetic improvement. Agronomy 11:1776. doi: 10.3390/agronomy11091776, PMID: PubMed DOI

Ramkissoon A., Ramsubhag A., Jayaraman J. (2017). Phytoelicitor activity of three Caribbean seaweed species on suppression of pathogenic infections in tomato plants. J. Appl. Phycol. 29, 3235–3244. doi: 10.1007/s10811-017-1160-0 DOI

Ray D. K., Mueller N. D., West P. C., Foley J. A. (2013). Yield trends are insufficient to double global crop production by 2050. PLoS One 8:e66428. doi: 10.1371/journal.pone.0066428, PMID: PubMed DOI PMC

Renzaglia K. S., Villareal J. C., Piatkowski B. T., Lucas J. R., Merced A. (2017). Hornwort stomata, architecture, and fate of shared with 400 million year old fossil plants without leaves. Plant Physiol. 174, 788–797. doi: 10.1104/pp.17.00156, PMID: PubMed DOI PMC

Robic A., Bertrand D., Sassi J.-F., Lerat Y., Lahaye M. (2009). Determination of the chemical composition of ulvan, a cell wall polysaccharide from Ulva spp. (Ulvales, Chlorophyta) by FT-IR and chemometrics. J. Appl. Phycol. 21, 451–456. doi: 10.1007/s10811-008-9390-9 DOI

Rouphael Y., Colla G. (2020). Editorial, biostimulants in agriculture. Front. Plant Sci. 11:40. doi: 10.3389/fpls.2020.00040, PMID: PubMed DOI PMC

Šašek V., Nováková M., Dobrev P. I., Valentová O., Burketová L. (2012a). Beta-aminobutyric acid protects Brassica napus plants from infection by Leptosphaeria maculans. Resistance induction or a direct antifungal effect? Eur. J. Plant Pathol. 133, 279–289. doi: 10.1007/s10658-011-9897-9 DOI

Šašek V., Nováková M., Jindřichová B., Bóka K., Valentová O., Burketová L. (2012b). Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus. Mol. Plant-Microbe Interact. 25, 1238–1250. doi: 10.1094/MPMI-02-12-0033-R, PMID: PubMed DOI

Seifert G. J., Roberts K. (2007). The biology of arabinogalactan proteins. Annu. Rev. Plant Biol. 58, 137–161. doi: 10.1146/annurev.arplant.58.032806.103801, PMID: PubMed DOI

Sharma H. S. S., Fleming C., Selby C., Rao J. R., Martin T. (2014). Plant biostimulants, a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses. J. Appl. Phycol. 26, 465–490. doi: 10.1007/s10811-013-0101-9 DOI

Shefer S., Lebendiker M., Finkelshtein A., Chamovitz D. A., Golberg A. (2022). Ulvan crude extract’s chemical and biophysical profile and its effect as a biostimulant on Arabidopsis thaliana. Algal Res. 62:102609. doi: 10.1016/j.algal.2021.102609 DOI

Shoubaky G., Salem E. A. (2016). Effect of abiotic stress on endogenous phytohormones profile in some seaweeds. Int. J. Pharmacogn. Phytochem. Res. 8, 124–134.

Showalter A. M. (2001). Arabinogalactan-proteins, structure, expression and function. Cell. Mol. Life Sci. 58, 1399–1417. doi: 10.1007/PL00000784, PMID: PubMed DOI PMC

Sørensen I., Pettolino F. A., Bacic A., Ralph J., Lu F., O’Neill M. A., et al. . (2011). The charophycean green algae provide insights into the early origins of plant cell walls. Plant J. 68, 201–211. doi: 10.1111/j.1365-313X.2011.04686.x, PMID: PubMed DOI

Stadnik M. J., Freitas M. B. (2014). Algal polysaccharides as source of plant resistance inducers. Trop. Plant Pathol. 39, 111–118. doi: 10.1590/S1982-56762014000200001 DOI

Staudacher E. (2012). Methylation—an uncommon modification of glycans. Biol. Chem. 393, 675–685. doi: 10.1515/hsz-2012-0132, PMID: PubMed DOI PMC

Steiner A. A. (1984). “The universal nutrient solution.” in The Sixth International Congress on “Soilless Culture.” Apr 29-May 5; Pudoc, Wageningen, The Netherlands, 633–650.

Tan L., Eberhard S., Pattathil S., Warder C., Glushka J., Yuan C., et al. . (2013). An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25, 270–287. doi: 10.1105/tpc.112.107334, PMID: PubMed DOI PMC

Temple H., Mortimer J. C., Tryfona T., Yu X., Lopez-Hernandez F., Sorieul M., et al. . (2019). Two members of the DUF579 family are responsible for arabinogalactan methylation in Arabidopsis. Plant Direct. 3:e00117. doi: 10.1002/pld3.117, PMID: PubMed DOI PMC

Templeton D. W., Quinn M., Van Wychen S., Hyman D., Laurens L. M. L. (2012). Separation and quantification of microalgal carbohydrates. J. Chromatogr. A 1270, 225–234. doi: 10.1016/j.chroma.2012.10.034, PMID: PubMed DOI

Thordal-Christensen H., Zhang Z., Wei Y., Collinge D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction. Plant J. 11, 1187–1194. doi: 10.1046/j.1365-313X.1997.11061187.x DOI

Torres M. A., Dangl J. L., Jones D. G. (2002). Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. PNAS 99, 517–522. doi: 10.1073/pnas.012452499, PMID: PubMed DOI PMC

Trdá L., Janda M., Macková D., Pospíchalová R., Dobrev P. I., Burketová L., et al. . (2019). Dual mode of the saponin aescin in plant protection, antifungal agent and plant defense elicitor. Front. Plant Sci. 10:1448. doi: 10.3389/fpls.2019.01448, PMID: PubMed DOI PMC

Van de Wouw A. P., Howlett B. J. (2020). Advances in understanding the Leptosphaeria maculans—Brassica pathosystem and their impact on disease management. Can. J. Plant Pathol. 42, 149–163. doi: 10.1080/07060661.2019.1643788 DOI

Van Loon L. C., Rep M., Pieterse C. M. J. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135–162. doi: 10.1146/annurev.phyto.44.070505.143425, PMID: PubMed DOI

Vieira H. H., Bagatini I. L., Guinart C. M., Vieira A. A. H., Vieira H. H., Bagatini I. L., et al. . (2016). tufA gene as molecular marker for freshwater Chlorophyceae. Algae 31, 155–165. doi: 10.4490/algae.2016.31.4.14, PMID: PubMed DOI

Villa-Rivera M. G., Cano-Camacho H., López-Romero E., Zavala-Páramo M. G. (2021). The role of Arabinogalactan type II degradation in plant-microbe interactions. Front. Plant Sci. 12:730543. doi: 10.3389/fmicb.2021.730543, PMID: PubMed DOI PMC

Waszczak C., Carmody M., Kangasjärvi J. (2018). Reactive oxygen species in plant signaling. Annu. Rev. Plant Biol. 69, 209–236. doi: 10.1146/annurev-arplant-042817-040322, PMID: PubMed DOI

Wichard T., Charrier B., Mineur F., Bothwell J. H., Clerck O. D., Coates J. C. (2015). The green seaweed Ulva, a model system to study morphogenesis. Front. Plant Sci. 6:72. doi: 10.3389/fpls.2015.00072, PMID: PubMed DOI PMC

Wiesel L., Newton A. C., Elliott I., Booty D., Gilroy E. M., Birch P. R. J., et al. . (2014). Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front. Plant Sci. 5:655. doi: 10.3389/fpls.2014.00655, PMID: PubMed DOI PMC

Yaich H., Garna H., Besbes S., Paquot M., Blecker C., Attia H. (2013). Effect of extraction conditions on the yield and purity of ulvan extracted from Ulva lactuca. Food Hydrocoll. 31, 375–382. doi: 10.1016/j.foodhyd.2012.11.013 DOI

Yang J., Duan G., Li C., Liu L., Han G., Zhang Y., et al. . (2019). The crosstalks between jasmonic acid and other plant hormone signaling highlight the involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses. Front. Plant Sci. 10:1349. doi: 10.3389/fpls.2019.01349, PMID: PubMed DOI PMC

Yemm E. W., Willis A. J. (1954). The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57, 508–514. doi: 10.1042/bj0570508, PMID: PubMed DOI PMC

Zipfel C., Robatzek S., Navarro L., Oakeley E., Jones J. D. G., Felix G., et al. . (2004). Bacterial disease resistance through flagellin perception in Arabidopsis. Nature 428, 764–767. doi: 10.1038/nature02485, PMID: PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...