Biodiversity Literature Repository

Submit to community
Liberated Data
Published January 31, 2021 | Version v1
Journal article Restricted

Evolutionary changes in the glucosinolate biosynthetic capacity in species representing Capsella, Camelina and Neslia genera

Authors/Creators

  • 1. * & Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704, Poznan´, Poland

Description

Czerniawski, Paweł, Piasecka, Anna, Bednarek, Paweł (2021): Evolutionary changes in the glucosinolate biosynthetic capacity in species representing Capsella, Camelina and Neslia genera. Phytochemistry (112571) 181: 1-14, DOI: 10.1016/j.phytochem.2020.112571, URL: http://dx.doi.org/10.1016/j.phytochem.2020.112571

Files

Restricted

The record is publicly accessible, but files are restricted. <a href="https://zenodo.org/account/settings/login?next=https://zenodo.org/records/8291107">Log in</a> to check if you have access.

Linked records

Additional details

Identifiers

LSID
urn:lsid:plazi.org:pub:FF97FF8AED79FFA28B43FFC5DD100E67

Has part
Figure: 10.5281/zenodo.8291109 (DOI)
Figure: 10.5281/zenodo.8291111 (DOI)
Figure: 10.5281/zenodo.8291113 (DOI)
Figure: 10.5281/zenodo.8291117 (DOI)
Figure: 10.5281/zenodo.8291119 (DOI)
Figure: 10.5281/zenodo.8291121 (DOI)
Figure: 10.5281/zenodo.8291123 (DOI)
Figure: 10.5281/zenodo.8291127 (DOI)

References

  • Agerbirk, N., Olsen, C., Chew, F., Orgaard, M., 2010. Variable glucosinolate profiles of Cardamine pratensis (Brassicaceae) with equal chromosome numbers. J. Agric. Food Chem. 58, 4693-4700.
  • Aires, A., Carvalho, R., 2017. Rapid separation of indole glucosinolates in roots of Chinese cabbage (Brassica rapa subsp. pekinensis) by high-performance liquid chromatography with diode array detection. Int. J. Anal. Chem. 2017, 5125329.
  • Amyot, L., McDowell, T., Martin, S.L., Renaud, J., Gruber, M.Y., Hannoufa, A., 2019. Assessment of antinutritional compounds and chemotaxonomic relationships between Camelina sativa and its wild relatives. J. Agric. Food Chem. 67, 796-806.
  • Bak, S., Tax, F.E., Feldmann, K.A., Galbraith, D.W., Feyereisen, R., 2001. CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13, 101-111.
  • Barth, C., Jander, G., 2006. Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant J. 46, 549-562.
  • Barton, K.E., Boege, K., 2017. Future directions in the ontogeny of plant defence: understanding the evolutionary causes and consequences. Ecol. Lett. 20, 403-411.
  • Bednarek, P., Pi´slewska-Bednarek, M., Svatoˇs, A., Schneider, B., Doubsky, J., Mansurova, M., Humphry, M., Consonni, C., Panstruga, R., Sanchez-Vallet, A., Molina, A., Schulze-Lefert, P., 2009. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323, 101-106.
  • Bednarek, P., Pi´slewska-Bednarek, M., Ver Loren van Themaat, E., Maddula, R.K., Svatoˇs, A., Schulze-Lefert, P., 2011. Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives. New Phytol. 192, 713-726.
  • Beekwilder, J., van Leeuwen, W., van Dam, N.M., Bertossi, M., Grandi, V., Mizzi, L., Soloviev, M., Szabados, L., Molthoff, J.W., Schipper, B., Verbocht, H., de Vos, R.C.H., Morandini, P., Aarts, M.G.M., Bovy, A., 2008. The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PloS One 3, e2068.
  • Benderoth, M., Pfalz, M., Kroymann, J., 2008. Methylthioalkylmalate synthases: genetics, ecology and evolution. Phytochemistry Rev. 8, 255-268.
  • Benderoth, M., Textor, S., Windsor, A.J., Mitchell-Olds, T., Gershenzon, J., Kroymann, J., 2006. Positive selection driving diversification in plant secondary metabolism. Proc. Natl. Acad. Sci. U.S.A. 103, 9118-9123.
  • Berhow, M.A., Polat, U., Glinski, J.A., Glensk, M., Vaughn, S.F., Isbell, T., Ayala-Diaz, I., Marek, L., Gardner, C., 2013. Optimized analysis and quantification of glucosinolates from Camelina sativa seeds by reverse-phase liquid chromatography. Ind. Crop. Prod. 43, 119-125.
  • Bianco, G., Pascale, R., Lelario, F., Bufo, S.A., Cataldi, T.R.I., 2016. The Investigation of Glucosinolates by Mass Spectrometry. Glucosinolates. Springer International Publishing, pp. 431-461.
  • Blaˇzevi´c, I., Montaut, S., Burˇcul, F., Olsen, C.E., Burow, M., Rollin, P., Agerbirk, N., 2020. Glucosinolate structural diversity, identification, chemical synthesis and metabolism in plants. Phytochemistry 169, 112100.
  • Brown, P.D., Tokuhisa, J.G., Reichelt, M., Gershenzon, J., 2003. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62, 471-481.
  • Hammerbacher, A., Vasstao, D.G., 2020. The phytopathogenic fungus Sclerotinia sclerotiorum detoxifies plant glucosinolate hydrolysis products via an isothiocyanate hydrolase. Nat. Commun. 11, 3090.
  • Clauss, M.J., Dietel, S., Schubert, G., Mitchell-Olds, T., 2006. Glucosinolate and trichome defenses in a natural Arabidopsis lyrata population. J. Chem. Ecol. 32, 2351-2373.
  • Cole, R.A., 1976. Isothiocyanates, nitriles and thiocyanates as products of autolysis of glucosinolates in Cruciferae. Phytochemistry 15, 759-762.
  • Conn, K.L., Browne, L.M., Tewari, J.P., Ayer, W.A., 1994. Resistance to Rhizoctonia solani and presence of antimicrobial compounds in Camelina sativa roots. J. Plant Biochem. Biotechnol. 3, 125-130.
  • Daxenbichler, M.E., Spencer, G.F., Carlson, D.G., Rose, G.B., Brinker, A.M., Powell, R.G., 1991. Glucosinolate composition of seeds from 297 species of wild plants. Phytochemistry 30, 2623-2638.
  • Fan, J., Crooks, C., Creissen, G., Hill, L., Fairhurst, S., Doerner, P., Lamb, C., 2011. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331, 1185.
  • Fu, L., Wang, M., Han, B., Tan, D., Sun, X., Zhang, J., 2016. Arabidopsis myrosinase genes AtTGG4 and AtTGG5 are root-tip specific and contribute to auxin biosynthesis and root-growth regulation. Int. J. Mol. Sci. 17, 892.
  • Gan, X., Hay, A., Kwantes, M., Haberer, G., Hallab, A., Ioio, R.D., Hofhuis, H., Pieper, B., Cartolano, M., Neumann, U., Nikolov, L.A., Song, B., Hajheidari, M., Briskine, R., Kougioumoutzi, E., Vlad, D., Broholm, S., Hein, J., Meksem, K., Lightfoot, D., Shimizu, K.K., Shimizu-Inatsugi, R., Imprialou, M., Kudrna, D., Wing, R., Sato, S., Huijser, P., Filatov, D., Mayer, K.F.X., Mott, R., Tsiantis, M., 2016. The Cardamine hirsuta genome offers insight into the evolution of morphological diversity. Native Plants 2, 161-167.
  • Geu-Flores, F., Moldrup, M.E., B¨ottcher, C., Olsen, C.E., Scheel, D., Halkier, B.A., 2011. Cytosolic γ- glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis. Plant Cell 23, 2456-2469.
  • Grubb, D.C., Brandon, Z.J., Ludwig-Muller, J., Masuno, M.N., Molinski, T.F., Abel, S., 2004. Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J. 40, 893-908.
  • Halkier, B.A., Gershenzon, J., 2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333.
  • Hansen, B.G., Kliebenstein, D.J., Halkier, B.A., 2007. Identification of a flavinmonooxygenase as the S -oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J. 50, 902-910.
  • Hiruma, K., Fukunaga, S., Bednarek, P., Pi´slewska-Bednarek, M., Watanabe, S., Narusaka, Y., Shirasu, K., Takano, Y., 2013. Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs. Proc. Natl. Acad. Sci. U.S.A. 110, 9589-9594.
  • Hiruma, K., Onozawa-Komori, M., Takahashi, F., Asakura, M., Bednarek, P., Okuno, T., Schulze-Lefert, P., Takano, Y., 2010. Entry mode-dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell 22, 2429-2443.
  • Hopkins, R.J., van Dam, N.M., van Loon, J.J.A., 2009. Role of glucosinolates in insectplant relationships and multitrophic interactions. Annu. Rev. Entomol. 54, 57-83.
  • Hu, T.T., Pattyn, P., Bakker, E.G., Cao, J., Cheng, J.-F., Clark, R.M., Fahlgren, N., Fawcett, J.A., Grimwood, J., Gundlach, H., Haberer, G., Hollister, J.D., Ossowski, S., Ottilar, R.P., Salamov, A.A., Schneeberger, K., Spannagl, M., Wang, X., Yang, L., Nasrallah, M.E., Bergelson, J., Carrington, J.C., Gaut, B.S., Schmutz, J., Mayer, K.F. X., Van de Peer, Y., Grigoriev, I.V., Nordborg, M., Weigel, D., Guo, Y.-L., 2011. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476-481.
  • Jensen, L.M., Halkier, B.A., Burow, M., 2014. How to discover a metabolic pathway? An update on gene identification in aliphatic glucosinolate biosynthesis, regulation and transport. Biol. Chem. 395, 529-543.
  • Kabouw, P., van der Putten, W.H., van Dam, N.M., Biere, A., 2010. Effects of intraspecific variation in white cabbage (Brassica oleracea var. capitata) on soil organisms. Plant Soil 336, 509-518.
  • Kagale, S., Koh, C., Nixon, J., Bollina, V., Clarke, W.E., Tuteja, R., Spillane, C., Robinson, S.J., Links, M.G., Clarke, C., Higgins, E.E., Huebert, T., Sharpe, A.G., Parkin, I.A.P., 2014. The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat. Commun. 5, 3706.
  • Katz, E., Bagchi, R., Jeschke, V., Rasmussen, A.R.M., Hopper, A., Burow, M., Estelle, M., Kliebenstein, D.J., 2020. Diverse allyl glucosinolate catabolites independently influence root growth and development. Plant Physiol. 183, 1376-1390.
  • Kettles, G.J., Drurey, C., Schoonbeek, H.-j., Maule, A.J., Hogenhout, S.A., 2013. Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol. 198, 1178-1190.
  • Kim, J.H., Lee, B.W., Schroeder, F.C., Jander, G., 2008. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J. 54, 1015-1026.
  • Kittipol, V., He, Z., Wang, L., Doheny-Adams, T., Langer, S., Bancroft, I., 2019. Genetic architecture of glucosinolate variation in Brassica napus. J. Plant Physiol. 240, 152988.
  • Kjaer, A., Schuster, A., 1972. Glucosinolates in seeds of Neslia paniculata. Phytochemistry 11, 3045-3048.
  • Kliebenstein, D.J., Kroymann, J., Brown, P., Figuth, A., Pedersen, D., Gershenzon, J., Mitchell-Olds, T., 2001. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126, 811-825.
  • Kroymann, J., Donnerhacke, S., Schnabelrauch, D., Mitchell-Olds, T., 2003. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc. Natl. Acad. Sci. U.S.A. 100, 14587-14592.
  • Lamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D.L., Garcia-Hernandez, M., Karthikeyan, A.S., Lee, C.H., Nelson, W.D., Ploetz, L., Singh, S., Wensel, A., Huala, E., 2011. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40, 1202-1210.
  • Lee, K.-C., Chan, W., Liang, Z., Liu, N., Zhao, Z., Lee, A.W.-M., Cai, Z., 2008. Rapid screening method for intact glucosinolates in Chinese medicinal herbs by using liquid chromatography coupled with electrospray ionization ion trap mass spectrometry in negative ion mode. Rapid Commun. Mass Spectrom. 22, 2825-2834.
  • Lehmann, T., Janowitz, T., S´anchez-Parra, B., Alonso, M.-M.P., Trompetter, I., Piotrowski, M., Pollmann, S., 2017. Arabidopsis NITRILASE 1 contributes to the regulation of root growth and development through modulation of auxin biosynthesis in seedlings. Front. Plant Sci. 8, 36.
  • Li, J., Hansen, B.G., Ober, J.A., Kliebenstein, D.J., Halkier, B.A., 2008. Subclade of flavinmonooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol. 148, 1721-1733.
  • Lin, L., Sun, J., Chen, P., Zhang, R.-W., Fan, X.-E., Li, L.-W., Harnly, J., 2014. Profiling of glucosinolates and flavonoids in Rorippa indica (Linn.) Hiern. (cruciferae) by UHPLC- PDA-ESI/HRMSn. J. Agric. Food Chem. 62, 6118-6129.
  • Malka, S.K., Cheng, Y., 2017. Possible interactions between the biosynthetic pathways of indole glucosinolate and auxin. Front. Plant Sci. 8, 2131.
  • Martinez-Ballesta, M., Moreno-Fern´andez, D., Castejon, D., Ochando, C., Morandini, P., Carvajal, M., 2015. The impact of the absence of aliphatic glucosinolates on water transport under salt stress in Arabidopsis thaliana. Front. Plant Sci. 6, 524.
  • Meldau, S., Erb, M., Baldwin, I.T., 2012. Defence on demand: mechanisms behind optimal defence patterns. Ann. Bot. 110, 1503-1514.
  • Mikkelsen, M., Hansen, C., Wittstock, U., Halkier, B., 2000. Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J. Biol. Chem. 275, 33712-33717.
  • Mikkelsen, M.D., Naur, P., Halkier, B.A., 2004. Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. Plant J. 37, 770-777.
  • Mikkelsen, M.D., Petersen, B.L., Glawischnig, E., Jensen, A.B., Andreasson, E., Halkier, B. A., 2003. Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol. 131, 298-308.
  • Naur, P., Petersen, B.L., Mikkelsen, M.D., Bak, S., Rasmussen, H., Olsen, C.E., Halkier, B. A., 2003. CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol. 133, 63-72.
  • Olsen, C.E., Huang, X.-C., Hansen, C.I.C., Cipollini, D., Orgaard, M., Matthes, A., Geu-Flores, F., Koch, M.A., Agerbirk, N., 2016. Glucosinolate diversity within a phylogenetic framework of the tribe Cardamineae (Brassicaceae) unraveled with HPLC-MS/MS and NMR-based analytical distinction of 70 desulfoglucosinolates. Phytochemistry 132, 33-56.
  • Padilla, G., Cartea, M.E., Velasco, P., de Haro, A., Ord´as, A., 2007. Variation of glucosinolates in vegetable crops of Brassica rapa. Phytochemistry 68, 536-545.
  • Pastorczyk, M., Bednarek, P., 2016. The function of glucosinolates and related metabolites in plant innate immunity. Adv. Bot. Res. 80, 171-198.
  • Petersen, B., Chen, S., Hansen, C., Olsen, C., Halkier, B., 2002. Composition and content of glucosinolates in developing Arabidopsis thaliana. Planta 214, 562-571.
  • Pfalz, M., Mikkelsen, M.D., Bednarek, P., Olsen, C.E., Halkier, B.A., Kroymann, J., 2011. Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell 23, 716-729.
  • Pfalz, M., Mukhaimar, M., Perreau, F., Kirk, J., Hansen, C.I.C., Olsen, C.E., Agerbirk, N., Kroymann, J., 2016. Methyl transfer in glucosinolate biosynthesis mediated by indole glucosinolate O-methyltransferase 5. Plant Physiol. 172, 2190-2203.
  • Pfalz, M., Vogel, H., Kroymann, J., 2009. The gene controlling the indole glucosinolate Modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21, 985-999.
  • Piotrowski, M., Schemenewitz, A., Lopukhina, A., Muller, A., Janowitz, T., Weiler, E., Oecking, C., 2005. Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure. J. Biol. Chem. 279, 50717-50725.
  • Potter, M.J., Vanstone, V.A., Davies, K.A., Kirkegaard, J.A., Rathjen, A.J., 1999. Reduced susceptibility of Brassica napus to Pratylenchus neglectus in plants with elevated root levels of 2-phenylethyl glucosinolate. J. Nematol. 31, 291-298.
  • Russo, R., Galasso, I., Reggiani, R., 2014. Variability in glucosinolate content among Camelina species. Am. J. Plant Sci. 5, 294-298.
  • Saatkamp, A., Affre, L., Dutoit, T., Poschlod, P., 2011. Germination traits explain soil seed persistence across species: the case of Mediterranean annual plants in cereal fields. Ann. Bot. 107, 415-426.
  • Sarwar, M., Kirkegaard, J.A., Wong, P.T.W., Desmarchelier, J.M., 1998. Biofumigation potential of brassicas. Plant Soil 201, 103-112.
  • Schranz, M.E., Manzaneda, A.J., Windsor, A.J., Clauss, M.J., Mitchell-Olds, T., 2009. Ecological genomics of Boechera stricta: identification of a QTL controlling the allocation of methionine- vs branched-chain amino acid-derived glucosinolates and levels of insect herbivory. Heredity 102, 465-474.
  • S´eguin-Swartz, G., Eynck, C., Gugel, R.K., Strelkov, S.E., Olivier, C.Y., Li, J.L., Klein- Gebbinck, H., Borhan, H., Caldwell, C.D., Falk, K.C., 2009. Diseases of Camelina sativa (false flax). J. Indian Dent. Assoc. 31, 375-386.
  • Slotte, T., Hazzouri, K.M., Agren, J.A., Koenig, D., Maumus, F., Guo, Y.-L., Steige, K., Platts, A.E., Escobar, J.S., Newman, L.K., Wang, W., Mand´akov´a, T., Vello, E., Smith, L.M., Henz, S.R., Steffen, J., Takuno, S., Brandvain, Y., Coop, G., Andolfatto, P., Hu, T.T., Blanchette, M., Clark, R.M., Quesneville, H., Nordborg, M., Gaut, B.S., Lysak, M.A., Jenkins, J., Grimwood, J., Chapman, J., Prochnik, S., Shu, S., Rokhsar, D., Schmutz, J., Weigel, D., Wright, S.I., 2013. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat. Genet. 45, 831-835.
  • Sonderby, I.E., Geu-Flores, F., Halkier, B.A., 2010. Biosynthesis of glucosinolates - gene discovery and beyond. Trends Plant Sci. 15, 283-290.
  • Soroka, J., Olivier, C., Grenkow, L., S´eguin-Swartz, G., 2014. Interactions between Camelina sativa (Brassicaceae) and insect pests of canola. Can. Entomol. 147, 193-214.
  • Stotz, H.U., Sawada, Y., Shimada, Y., Hirai, M.Y., Sasaki, E., Krischke, M., Brown, P.D., Saito, K., Kamiya, Y., 2011. Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. Plant J. 67, 81-93.
  • Thomma, B.P.H.J., Nelissen, I., Eggermont, K., Broekaert, W.F., 1999. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J. 19, 163-171.
  • Ting, H.-M., Cheah, B.H., Chen, Y.-C., Yeh, P.-M., Cheng, C.-P., Yeo, F.K.S., Vie, A.K., Rohloff, J., Winge, P., Bones, A.M., Kissen, R., 2020. The role of a glucosinolate-derived nitrile in plant immune responses. Front. Plant Sci. 11, 257.
  • van Dam, N.M., 2009. Belowground herbivory and plant defenses. Annu. Rev. Ecol. Evol. Syst. 40, 373-391.
  • Vik, D., Mitarai, N., Wulff, N., Halkier, B.A., Burow, M., 2018. Dynamic modeling of indole glucosinolate hydrolysis and its impact on auxin signaling. Front. Plant Sci. 9, 550.
  • Windsor, A.J., Reichelt, M., Figuth, A., Svatoˇs, A., Kroymann, J., Kliebenstein, D.J., Gershenzon, J., Mitchell-Olds, T., 2005. Geographic and evolutionary diversification of glucosinolates among near relatives of Arabidopsis thaliana (Brassicaceae). Phytochemistry 66, 1321-1333.
  • Wittstock, U., Kurzbach, E., Herfurth, A.M., Stauber, E.J., 2016. Glucosinolate breakdown. Adv. Bot. Res. 80, 125-169.
  • Yamane, A., Fujikura, J., Ogawa, H., Mizutani, J., 1992. Isothiocyanates as alleopathic compounds from Rorippa indica Hiern. (Cruciferae) roots. J. Chem. Ecol. 18, 1941-1954.
  • Yuan, D., Shim, Y.Y., Shen, J., Jadhav, P.D., Meda, V., Reaney, M.J.T., 2017. Distribution of glucosinolates in Camelina seed fractions by HPLC-ESI-MS/MS. Eur. J. Lipid Sci. Technol. 119, 1600040.
  • Zhang, J., Wang, X., Cheng, F., Wu, J., Liang, J., Yang, W., Wang, X., 2015. Lineagespecific evolution of Methylthioalkylmalate synthases (MAMs) involved in glucosinolates biosynthesis. Front. Plant Sci. 6, 18.
  • Zhao, Z., Zhang, W., Stanley, B.A., Assmann, S.M., 2008. Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell 20, 3210-3226.
  • Zust, T., Agrawal, A.A., 2017. Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu. Rev. Plant Biol. 68, 513-534.
  • Zust, T., Strickler, S.R., Powell, A.F., Mabry, M.E., An, H., Mirzaei, M., York, T., Holland, C.K., Kumar, P., Erb, M., Petschenka, G., G´omez, J.-M., Perfectti, F., Muller, C., Pires, J.C., Mueller, L.A., Jander, G., 2020. Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae). eLife 9, e51712.