Piriformospora indica cell wall modulates gene expression and metabolite profile in Linum album hairy roots

Ahmadi-Sakha S, Sharifi M, Niknam V (2016) Bioproduction of phenylethanoid glycosides by plant cell culture of Scrophularia striata Boiss.: from shake-flasks to bioreactor. Plant Cell Tissue Organ Cult 124(2):275–281 Ahsan N, Nakamura T, Komatsu S (2012) Differential responses of microsomal proteins and metabolites in two contrasting cadmium (Cd)-accumulating soybean cultivars under Cd stress. Amino Acids 42:317–327 Angelovici R, Fait A, Zhu X, Szymanski J, Feldmesser E, Fernie AR, Galili G (2009) Deciphering transcriptional and metabolic networks associated with lysine metabolism during Arabidopsis seed development. Plant Physiol 151:2058–2072 Babar Ali M, Singh N, Shohael AM, Hahn EJ, Paek KY (2006) Phenolics metabolism and lignin synthesis in root suspension cultures of Panax ginseng in response to copper stress. Plant Sci 171:147–154 Baldi A, Jain A, Gupta N, Srivastava AK, Bisaria VS (2008) Co-culture of arbuscular mycorrhiza-like fungi (Piriformospora indica and Sebacina vermifera) with plant cells of Linum album for enhanced production of podophyllotoxins: a first report. Biotechnol Lett 30(9):1671 Baldi A, Farkya S, Jain A, Gupta N, Mehra R, Datta V, Srivastava AK, Bisaria VS (2010) Enhanced production of podophyllotoxins by co-culture of transformed Linum album cells with plant growth-promoting fungi. Pure Appl Chem 82(1):227–241 Biermann M, Bardl B, Vollstadt S, Linnemann J, Knüpfer U, Seidel G, Horn U (2013) Simultaneous analysis of the non-canonical amino acids norleucine and norvaline in biopharmaceutical-related fermentation processes by a new ultra high performance liquid chromatography approach. Amino Acids 44:1225–1231 Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254 Campbell MM, Ellis BE (1992) Fungal elicitor-mediated responses in pine cell cultures: cell wall-bound phenolics. Phytochemistry 31:737–742 Chashmi NA, Sharifi M, Yousefzadi M, Behmanesh M, Rezadoost H, Cardillo A, Palazon J (2013) Analysis of 6-methoxy podophyllotoxin and podophyllotoxin in hairy root cultures of Linum album Kotschy ex Boiss. Med Chem Res 22:745–752 Corbin C, Drouet S, Mateljak I, Markulin L, Decourtil C, Renouard S, Lopez T, Doussot J, Lamblin F, Auguin D, Lainé E (2017) Functional characterization of the pinoresinol-lariciresinol reductase-2 gene reveals its roles in yatein biosynthesis and flax defense response. Planta 246:405–420 Cvikrová M, Malá J, Hrubcová M, Eder J, Foretová S (2008) Induced changes in phenolic acids and stilbenes in embryogenic cell cultures of Norway spruce by culture filtrate of Ascocalyx abietina. J Plant Dis Protect 115(2):57–62 De Ascensao AR, Dubery IA (2003) Soluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f.sp. cubense. Phytochemistry 63:679–686 De Pietro A, Rosales RP, Luque-Gracia JL, Martines lopez R, Gil C (2009) The Fusarium oxysporum cell wall proteome under adhesion-inducing conditions. Proteomics 9:4755–4769 Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Me´rillon JM, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140:499–511 Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455–463 Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097 Esmaeilzadeh Bahabadi S, Sharifi M, Safaie N, Murata J, Yamagaki T, Satake H (2011) Increased lignan biosynthesis in the suspension cultures of Linum album by fungal extracts. Plant Biotechnol Rep 5:367–373 Esmaeilzadeh S, Sharifi M, Behmanesh M, Safaei N, Murata J, Araki R, Yamagaki T, Satake H (2012) Time-course changes in fungal elicitor-induced lignan synthesis and expression of the relevant genes in cell cultures of Linum album. J Plant Physiol 169:487–491 Esmaeilzadeh S, Sharifi M, Ahmadian CN, Murata J, Satake H (2014) Significant enhancement of lignan accumulation in hairy root cultures of Linum album using biotic elicitors. Acta Physiol Plant 36:3325–3331 Federolf K, Alfermann AW, Fuss E (2004) Aryltetralin-lignan formation in two different cell lines of Linum album: deoxypodophyllotoxin 6-hydroxylase, a key enzyme for the formation of 6-methoxypodophyllotoxin. Phytochemistry 68:1397–1406 Fuss E (2003) Lignans in plant cell and organ cultures: an overview. Photochem Rev 2:307–320 Gangopadhyay M, Dewanjee S, Bhattacharya S (2011) Enhanced plumbagin production in elicited Plumbago indica hairy root cultures. J Biosci Bioeng 111(6):706–710 Garden HJ (2003) Biotechnological production of podophyllotoxin by Linum album suspension cultures. [Doctoral thesis] Heinrich-Heine Universität, Düsseldorf Ghanati F, Morita A, Yokota H (2005) Deposition of suberin induced by excess boron. Plant Sci 168:397–405 Grayer RJ, Kokubun T (2001) Plant-fungal interactions: the search of phytoalexins and other antifungal compounds from higher plants. Phytochemistry 56:253–263 Gudej J, Tomczyk M (2004) Determination of flavonoids, tannins and ellagic acid in leaves from Rubus L. species. Arch Pharm Res 27(11):1114–1119 Hano C, Addi M, Bensaddek L, Baltora-Rosset S, Doussot J, Maury S, Mesnard F, Chabbert B, Hawkins S, Laine E, Lamblin F (2006) Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta 223:975–989 Iiyama K, Wallis FA (1990) Determination of lignin in herbaceous plants by an improved acetyl bromide procedure. J Sci Food Agric 51:145–161 Kamalipourazad M, Sharifi M, Maivan HZ, Behmanesh M, Chashmi NA (2016) Induction of aromatic amino acids and phenylpropanoid compounds in Scrophularia striata Boiss. cell culture in response to chitosan-induced oxidative stress. Plant Physiol Biochem 107:374–384 Keinänen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J Agric Food Chem 49:3553–3558 Khan W, Prithiviraj B, Donald L, Smith J (2003) Chitosan and chitin oligomers increase phenylalanine ammonia-lyase and tyrosine ammonia-lyase activities in soybean leaves. Plant Physiol 160:859–863 Komaraiah P, Amrutha RN, Kishor PBK, Ramakrishna SV (2002) Elicitor enhanced production of plumbagin in suspension cultures of Plumbago rosea L. Enzyme Microb Technol 31(5):634–639 Kumar V, Rajauria G, Sahai V, Bisaria VS (2012) Culture filtrate of root endophytic fungus Piriformospora indica promotes the growth and lignan production of Linum album hairy root cultures. Process Biochem 47:901–907 Kumar P, Chaturvedi R, Sundar D, Bisaria VS (2016) Piriformospora indica enhances the production of pentacyclic triterpenoids in Lantana camara L. suspension cultures. Plant Cell, Tissue Organ Cult 125(1):23–29 Moss GP (2000) Nomenclature of lignans and neolignans (IUPAC Recommendations 2000). Pure Appl Chem 72:1493–1523 Muranaka T, Miyata M, Ito K, Tachibana S (1998) Production of podophyllotoxin in Juniperus chinensis callus cultures treated with oligosaccharides and a biogenetic precursor. Phytochemistry 49(2):491–496 Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay of tobacco tissue culture. Physiol Plant 15:473–497 Owen RW, Haubner R, Mier W, Giacosa A, Hull WE, Spiegelhalder B, Bartsch H (2003) Isolation, structure elucidation and antioxidant potential of the major phenolic and flavonoid compounds in brined olive drupes. Food Chem Toxicol 41:703–717 Poschenrieder C, Tolra R, Barcelό J (2006) Can metals defend plants against biotic stress? Trends Plant Sci 11:288–295 Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification tool-box in Arabidopsis. Plant Physiol 133:1051–1071 Saxena P, Ahlawat S, Ali A, Khan S, Abdin MZ (2017) Gene expression analysis of the withanolide biosynthetic pathway in hairy root cultures of Withania somnifera elicited with methyl jasmonate and the fungus Piriformospora indica. Symbiosis 71(2):143–154 Shaheen S, Nasee S, Ashraf M, Akram AA (2013) Salt stress affects water relations, photosynthesis, and oxidative defense mechanisms in Solanum melongena L. J Plant Interact 8:85–96 Sreelakshmi Y, Sharma R (2008) Differential regulation of phenylalanine ammonia lyase activity and protein level by light in tomato seedlings. Plant Physiol Biochem 46:444–451 Taguchi G, Yazawa T, Hayashida N, Okazaki M (2001) Molecular cloning and heterologous expression of novel glucosyltransferases from tobacco cultured cells that have broad substrate specificity and are induced by salicylic acid and auxin. Eur J Biochem 268:4086–4094 Tahsili J, Sharifi M, Safaie N, Esmaeilzadeh-Bahabadi S, Behmanesh M (2014) Induction of lignans and phenolic compounds in cell culture of Linum album by culture filtrate of Fusarium graminearum. J Plant Interact 9(1):412–417 Tashackori H, Sharifi M, Chashmi NA, Safaie N, Behmanesh M (2016) Induced-differential changes on lignan and phenolic acid compounds in Linum album hairy roots by fungal extract of Piriformospora indica. Plant Cell, Tissue Organ Cult 127(1):187–194 Valletta A, De Angelis G, Badiali C, Brasili E, Miccheli A, Di Cocco ME, Pasqua G (2016) Acetic acid acts as an elicitor exerting a chitosan-like effect on xanthone biosynthesis in Hypericum perforatum L. root cultures. Plant Cell Rep 35(5):1009–1020 Vardapetyan HR, Kirakosyan AB, Oganesyan AA, Penesyan AR, Alfermann WA (2003) Effect of various elicitors on lignan biosynthesis in callus cultures of Linum austriacum. Russ J Plant Physiol 50:297–300 Vasconsuelo A, Boland R (2007) Molecular aspects of the early stages of secondary metabolites in plants. Plant Sci 172:861–875 Vicent MRS, Plasencia J (2011) Salicylic acid beyond defense: its role in plant growth and development. J Exp Bot 62:3321–3338 Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20 Wang J, Zheng L, Wu J, Tan R (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide 15:351–358 Ward JL, Forcat S, Beckmann M, Bennett M, Miller SJ, Baker JM, Hawkins ND, Vermeer CP, Lu C, Lin W, Truman WM (2010) The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J 63(3):443–457 Wen PF, Chen JY, Wan SB, Kong WF, Zhang P, Wang W, Zhan JC, Pan Q, Huang WD (2008) Salicylic acid activates phenylalanine ammonia-lyase in grape berry in response to high temperature stress. Plant Growth Regul 55:1–10 Westcott ND, Muir AD (2003) Flax seed lignan in disease prevention and health promotion. Phytochem Rev 2:401–417 Yousefzadi M, Sharifi M, Behmanesh M, Moyano E, Palazon J (2010a) Salicylic acid improves podophyllotoxin production in cell cultures of Linum album by increasing the expression of genes related with its biosynthesis. Biotechnol Lett 32(11):1739–1743 Yousefzadi M, Sharifi M, Chashmi NA, Behmanesh M, Ghasempour A (2010b) Optimization of podophyllotoxin extraction method from Linum album cell cultures. Pharm Biol 48(12):1421–1425 Yousefzadi M, Sharifi M, Behmanesh M, Ghasempour A, Moyano E, Palazon J (2012) The effect of light on gene expression and podophyllotoxin biosynthesis in Linum album cell culture. Plant Physiol Biochem 56:41–46 Zabala G, Zou J, Tuteja J, Gonzalez DO, Clough SJ, Vodkin LO (2006) Transcriptome changes in the phenylpropanoid pathway of Glycine max in response to Pseudomonas syringae infection. BMC Plant Biol 6(1):26 Zafari S, Sharifi M, Ahmadian Chashmi N, Mur LA (2016) Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds and amino acids. Plant Physiol Biochem 99:11–20 Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333