Abstract
Inositol and its’ metabolic derivatives such as galactinol, raffinose, methylated inositols etc. are well known significant osmoprotectants produced in response to various abiotic stresses in plants. The present work focuses on the importance of phylogenetic analysis in search of a presumptive ‘master switch’ involved in inducing a set of stress-responsive coregulated genes in the pathways involved in inositol synthesis and its further metabolism. It can be reasonably assumed that the entire network of genes induced under a particular stress is governed by a few common stress-responsive transcription factor binding sites or cis elements in their respective promoters. A phylogenetic analysis of such regulatory regions of the coregulated genes participating in entire inositol metabolic pathway throughout evolution, can form a novel approach in recognizing the conserved stress-regulatory signature(s) or ‘master switch(es)’ regulating this important pathway under the stress impact.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
All data are available.
Code availability
Not Applicable.
Abbreviations
- Ino1 or MIPS:
-
L-myo-inositol-1-phosphate synthase
- IMT:
-
Inositol methyl transferase
- GolS:
-
Galactinol synthase
- RafS:
-
Raffinose synthase
- StaS:
-
Stachyose synthase
- PLC:
-
Phospholipase C
- MIOX:
-
Myo-inositol oxygenase
- IP6K:
-
Inositol hexakisphosphate kinase
- CAREs:
-
Cis-acting regulatory elements
- TF:
-
Transcription factor
- TFBS:
-
Transcription factor binding site
References
Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid- regulated gene expression. Plant Cell 9(10):1859–1868. https://doi.org/10.1105/tpc.9.10.1859
Abreu EFM, Aragão FJL (2007) Isolation and characterization of a myo-inositol-1-phosphate synthase gene from yellow passion fruit (Passiflora edulis f. flavicarpa) expressed during seed development and environmental stress. Ann Bot 99(2):285–292. https://doi.org/10.1093/aob/mcl256
Adepoju O, Williams SP, Craige B (2019) Inositol trisphosphate kinase and diphosphoinositol pentakisphosphate kinase enzymes constitute the inositol pyrophosphate synthesis pathway in plants. bioRxiv 724914. https://doi.org/10.1101/724914
Agarwal R, Mumtaz H, Ali N (2009) Role of inositol polyphosphates in programmed cell death. Mol Cell Biochem 328(1–2):155–165. https://doi.org/10.1007/s11010-009-0085-6
Ahn CH, Hossain A, Lee E, Kanth BK, Park PH (2018) Increased salt and drought tolerance by D-pinitol production in transgenic Arabidopsis thaliana. Biochem Biophys Res Commun 504:315–320. https://doi.org/10.1016/j.bbrc.2018.08.183
Arif MA, Alseekh S, Harb J, Fernie A, Frank W (2018) Abscisic acid, cold and salt stimulate conserved metabolic regulation in the moss Physcomitrella patens. Plant Biol 20:1014–1022. https://doi.org/10.1111/plb.12871
Arisz SA, Valianpour F, van Gennip AH, Munnik T (2003) Substrate preference of stress-activated phospholipase D in Chlamydomonas and its contribution to PA formation. Plant J 34:595–604. https://doi.org/10.1046/j.1365-313x.2003.01750.x
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713. https://doi.org/10.1007/BF00029852
Basak A, Jha TB, Adhikari J (2012) Biosynthesis of myo-inositol in lycopods: characteristics of the pteridophytic L-myo-inositol-1-phosphate synthase and myo-inositol-1-phosphate phosphatase from the strobili of Lycopodium clavatum and Selaginella monospora. Acta Physiol Plant 34:1579–1582. https://doi.org/10.1007/s11738-012-0924-z
Basak P, Maitra-Majee S, Das JK, Mukherjee A, Ghosh Dastidar S, Choudhury PP, Majumder AL (2017) An evolutionary analysis identifies a conserved pentapeptide stretch containing the two essential lysine residues for rice L-myo-inositol 1-phosphate synthase catalytic activity. PLoSOne 12(9):e0185351. https://doi.org/10.1371/journal.pone.0185351
Basak P, Sangma S, Mukherjee A, Agarwal T, Sengupta S, Ray S, Majumder AL (2018) Functional characterization of two myo-inositol-1-phosphate synthase (MIPS) gene promoters from the halophytic wild rice (Porteresia coarctata). Planta 248(5):1121–1141. https://doi.org/10.1007/s00425-018-2957-z
Becker GW, Lester RL (1977) Changes in phospholipids of Saccharomyces cerevisiae associated with inositol-less death. J Biol Chem 252:8684–8691
Belgaroui N, Lacombe B, Rouached H, Hanin M (2018) Phytase overexpression in Arabidopsis improves plant growth under osmotic stress and in combination with phosphate deficiency. Sci Rep 8(1):1137. https://doi.org/10.1038/s41598-018-19493-w
Benaroya RO, Zamski E, Tel-Or E (2004) L-myo-inositol-1- phosphate synthase in the aquatic fern Azolla filiculoides. Plant Physiol Biochem 42:97–102. https://doi.org/10.1016/j.plaphy.2003.11.008
Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:581–585. https://doi.org/10.1126/science.1197985
Buchanan CD, Lim S, Salzman RA et al (2005) Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol 58(5):699–720. https://doi.org/10.1007/s11103-005-7876-2
Chatterjee J, Majumder AL (2010) Salt-induced abnormalities on root tip mitotic cells of Allium cepa: prevention by inositol pretreatment. Protoplasma 245:165–172. https://doi.org/10.1007/s00709-010-0170-4
Chatterjee A, Majee M, Ghosh S, Majumder AL (2004) sll1722, an unassigned open reading frame of Synechocystis PCC 6803, codes for L-myo-inositol 1-phosphate synthase. Planta 218(6):989–998. https://doi.org/10.1007/s00425-003-1190-5
Chatterjee A, Dastidar KG, Maitra S, Das-Chatterjee A, Dihazi H, Eschrich K, Majumder AL (2006) sll1981, an acetolactate synthase homologue of Synechocystis sp. PCC6803, functions as L-myo-inositol 1-phosphate synthase. Planta 224(2):367–379. https://doi.org/10.1007/s00425-006-0221-4
Chettri DR, Mukherjee AK, Adhikari J (2006) Partial purification and characterization of L-myo-inositol-1-phosphate synthase of pteridophytic origin. Acta Physiol Plant 28:101–107. https://doi.org/10.1007/s11738-006-0036-8
Couso I, Evans BS, Li J et al (2016) Synergism between inositol polyphosphates and TOR Kinase signaling in nutrient sensing, growth control, and lipid metabolism in Chlamydomonas. Plant Cell 28(9):2026–2042. https://doi.org/10.1105/tpc.16.00351
Culbertson MR, Henry SA (1975) Inositol requiring mutants of Saccharomyces cerevisiae. Genetics 80:23–40
Das P, Datta S, Samanta MK, Mukherjee A, Majumder AL (2017) Phosphoinositides and phospholipase C signalling in plant stress response - a revisit. Proc Indian Natn Sci Acad 83(4):845–863. https://doi.org/10.16943/ptinsa/2017/49223
Das-Chatterjee A, Goswami L, Maitra S, Dastidar KG, Ray S, Majumder AL (2006) Introgression of a novel salt-tolerant L-myo-inositol 1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka (PcINO1) confers salt tolerance to evolutionary diverse organisms. FEBS Lett 580(16):3980–3988. https://doi.org/10.1016/j.febslet.2006.06.033
Dastidar KG, Maitra S, Goswami L, Roy D, Das KP, Majumder AL (2006) An insight into the molecular basis of salt tolerance of L-myo-inositol 1-P synthase (PcINO1) from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. Plant Physiol 140(4):1279–1296
De Bodt S, Thiessen G, Van de Peer Y (2006) Promoter analysis of MADS-box genes in eudicots through phylogenetic footprinting. Mol Biol Evol 23(6):1293–1303. https://doi.org/10.1093/molbev/msk016
de Oliveira DF, de Lopes L, Gomes-Filho E (2020) Metabolic changes associated with differential salt tolerance in sorghum genotypes. Planta 252:34. https://doi.org/10.1007/s00425-020-03437-8
Dean-Johnson M, Henry SA (1989) Biosynthesis of inositol in yeast: primary structure of myo-inositol-1-phosphate synthase (EC 5514) and functional analysis of its structural gene the INO1 locus. J Biol Chem 264(2):1274–1283
Deng X, Yuan S, Cao H et al (2019) Phosphatidylinositol-hydrolyzing phospholipase C4 modulates rice response to salt and drought. Plant Cell Environ 42:536–548. https://doi.org/10.1111/pce.13437
Desai M, Rangarajan P, Donahue JL et al (2014) Two inositol hexakisphosphate kinases drive inositol pyrophosphate synthesis in plants. Plant J 80(4):642–653. https://doi.org/10.1111/tpj.12669
Donahue TF, Henry SA (1981) myo-Inositol-1-phosphate synthase. Characteristics of the enzyme and identification of its structural gene in yeast. J Biol Chem 10(256):7077–7085
Duan JZ, Zhang MH, Zhang HL et al (2012) OsMIOX, a myo-inositol oxygenase gene, improves drought tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Plant Sci 196:143–151
Dumschott K, Dechorgnat J, Merchant A (2019) Water deficit elicits a transcriptional response of genes governing d-pinitol biosynthesis in soybean (Glycine max). Int J Mol Sci 20(10):2411. https://doi.org/10.3390/ijms20102411
Egert A, Keller F, Peters S (2013) Abiotic stress-induced accumulation of raffinose in Arabidopsis leaves is mediated by a single raffinose synthase (RS5, At5g40390). BMC Plant Biol 13:218. https://doi.org/10.1186/1471-2229-13-218
Fujita M, Fujita Y, Maruyama K et al (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39(6):863–876. https://doi.org/10.1111/j.1365-313X.2004.02171.x
Geiger D, Scherzer S, Mumm P et al (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107(17):8023–8028. https://doi.org/10.1073/pnas.0912030107
Ghars MA, Richard L, Vos DL et al (2012) Phospholipases C and D modulate proline accumulation in Thellungiella halophila/salsuginea differently according to the severity of salt or hyperosmotic stress. Plant Cell Environ 53(1):183–192. https://doi.org/10.1093/pcp/pcr164
Gómez-Muñoz A, Kong JY, Parhar K et al (2005) Ceramide-1-phosphate promotes cell survival through activation of the phosphatidylinositol 3-kinase/protein kinase B pathway. FEBS Lett 579(17):3744–3750. https://doi.org/10.1016/j.febslet.2005.05.067
Goswami L, Sengupta S, Mukherjee S, Ray S, Mukherjee R, Majumder AL (2014) Targeted expression of L-myo-inositol 1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka confers multiple stress tolerance in transgenic crop plants. J Plant Biochem Biotech 23:316–330. https://doi.org/10.1007/s13562-013-0217-7
Hait NC, RayChaudhuri A, Das A, Bhattacharyya S, Majumder AL (2002) Processing and activation of chloroplast L-myo-inositol 1-phosphate synthase from Oryza sativa requires signals from both light and salt. Plant Sci 162(4):559–568. https://doi.org/10.1016/S0168-9452(01)00591-X
Hartung W (2010) The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37:806–812. https://doi.org/10.1071/FP10058
Hartung W, Gimmler H (1994) A stress physiological role for abscisic acid (ABA) in lower plants. In: Behnke HD, Lüttge U, Esser K, Kadereit JW, Runge M (eds) Progress in botany. Springer, Berlin, pp 157–173. https://doi.org/10.1007/978-3-642-78568-9_9
Hartung W, Weiler EW, Volk OH (1987) Immunochemical evidence that abscisic acid is produced by several species of Anthocerotae and Marchantiales. Bryologist 90(4):393–400. https://doi.org/10.2307/3243104
Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21(9):R346–R355. https://doi.org/10.1016/j.cub.2011.03.015
Hazra A, Dasgupta N, Sengupta C, Das S (2019) MIPS: Functional dynamics in evolutionary pathways of plant kingdom. Genomics 111:1929–1945. https://doi.org/10.1016/j.ygeno.2019.01.004
Hellwege E, Dietz K, Volk O, Hartung W (1994) Abscisic acid and the induction of desiccation tolerance in the extremely xerophilic liverwort Exormotheca holstii. Planta 194(4):525–531
Henry SA, Atkinson KD, Kolat AI, Culbertson MR (1977) Growth and metabolism of inositol-starved Saccharomyces cerevisiae. J Bacteriol 130(1):472–484
Hirayama T, Ohto C, Mizoguchi T, Shinozaki K (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Indian Natn Sci Acad 92(9):3903–3907. https://doi.org/10.1073/pnas.92.9.3903
Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. Plant J 9(4):537–548. https://doi.org/10.1046/j.1365-313x.1996.09040537.x
Jansen K, Du B, Kayler Z et al (2014) Douglas-fir seedlings exhibit metabolic responses to increased temperature and atmospheric drought. PLoS ONE 9(12):e114165. https://doi.org/10.1371/journal.pone.0114165
Jeong JS, Kim YS, Baek KH et al (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197. https://doi.org/10.1104/pp.110.154773
Jeong JS, Kim YS, Redillas MC et al (2013) OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol J 11:101–114. https://doi.org/10.1111/pbi.12011
Jia Q, Kong D, Li Q et al (2019) The function of inositol phosphatases in plant tolerance to abiotic stress. Int J Mol Sci 20(16):3999. https://doi.org/10.3390/ijms20163999
Jiang Y, Deyholos M (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105. https://doi.org/10.1007/s11103-008-9408-3
Joo J, Lee YH, Song SI (2014) Overexpression of the rice basic leucine zipper transcription factor OsbZIP12 confers drought tolerance to rice and makes seedlings hypersensitive to ABA. Plant Biotechnol Rep 8:431–441. https://doi.org/10.1007/s11816-014-0335-2
Jung H, Lee DK, Choi YD, Kim JK (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci 236:304–312. https://doi.org/10.1016/j.plantsci.2015.04.018
Jung H, Chung PJ, Park SH, Redillas MCFR, Kim YS, Suh JW, Kim JK (2017) Overexpression of OsERF48 causes regulation of OsCML16, a calmodulin-like protein gene that enhances root growth and drought tolerance. Plant Biotechnol J 15(10):1295–1308. https://doi.org/10.1111/pbi.12716
Kaur H, Verma P, Petla BP, Rao V, Saxena SC, Majee M (2013) Ectopic expression of ABA-inducible dehydration-responsive chickpea l-myo-inositol 1-phosphate synthase 2 (CaMIPS2) in Arabidopsis enhances tolerance to salinity and dehydration stress. Planta 237(1):327–335. https://doi.org/10.1007/s00425-012-1781-0
Ke M, Zheng Y, Zhu Z (2015) Rethinking the origin of auxin biosynthesis in plants. Front Plant Sci 6:1093. https://doi.org/10.3389/fpls.2015.01093
Keith AD, Pollard EC, Snipes W (1977) Inositol-less death in yeast results in a simultaneous increase in intracellular viscosity. Biophys J 17(3):205–212. https://doi.org/10.1016/S0006-3495(77)85650-6
Keller R, Brearley CA, Trethewey RN, Muller-Rober B (1998) Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol 3-phosphate synthase. Plant J 16(4):403–410. https://doi.org/10.1046/j.1365-313x.1998.00309.x
Kerhornou A, Guigo R (2007) BioMoby web services to support clustering of coregulated genes based on similarity of promoter configurations. Bioinformatics 23(14):1831–1833. https://doi.org/10.1093/bioinformatics/btm252
Khurana N, Chauhan H, Khurana P (2012) Expression analysis of a heat-inducible, Myo-inositol-1 phosphate synthase (MIPS) gene from wheat and the alternatively spliced variants of rice and Arabidopsis. Plant Cell Rep 31(1):237–251. https://doi.org/10.1007/s00299-011-1160-5
Kim JI, Baek D, Park HC et al (2013) Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Mol Plant 6(2):337–349. https://doi.org/10.1093/mp/sss100
Klig LS, Henry SA (1984) Isolation of the yeast INO1 gene: located on an autonomously replicated plasmid, the gene is fully regulated. Proc Natl Acad Sci 81(12):3816–3820. https://doi.org/10.1073/pnas.81.12.3816
Kong W, Gong Z, Zhong H et al (2019) Expansion and evolutionary patterns of glycosyltransferase family 8 in gramineae crop genomes and their expression under salt and cold stresses in Oryza sativa ssp. japonica. Biomolecules 9(5):188. https://doi.org/10.3390/biom9050188
Kumar V, Thakur JK, Prasad M (2021) Histone acetylation dynamics regulating plant development and stress responses. Cell Mol Life Sci. https://doi.org/10.1007/s00018-021-03794-x
Kuo TM, Lowell CA, Nelsen TC (1997) Occurrence of pinitol in developing soybean seed tissues. Phytochemistry 45(1):29–35. https://doi.org/10.1016/S0031-9422(96)00795-9
Laha D, Parvin N, Hofer A et al (2019) Arabidopsis ITPK1 and ITPK2 Have an evolutionarily conserved phytic acid kinase activity. ACS Chem Biol 4(10):2127–2133. https://doi.org/10.1021/acschembio.9b00423
Lee YP, Babakov A, de Boer B et al (2012) Comparison of freezing tolerance, compatible solutes and polyamines in geographically diverse collections of Thellungiella sp. and Arabidopsis thaliana accessions. BMC Plant Biol 12:131. https://doi.org/10.1186/1471-2229-12-131
Lee DK, Jung H, Jang G et al (2016) Overexpression of the OsERF71 transcription factor alters rice root structure and drought resistance. Plant Physiol 172(1):575–588. https://doi.org/10.1104/pp.16.00379
Lisko KA, Torres R, Harris RS et al (2013) Elevating vitamin C content via overexpression of myo-inositol oxygenase and L-gulono-1,4-lactone oxidase in Arabidopsis leads to enhanced biomass and tolerance to abiotic stresses. In Vitro Cell Dev Biol -Plant 49:643–655. https://doi.org/10.1007/s11627-013-9568-y
Liu Q, Kasuga M, Sakuma Y et al (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively. Arabidopsis Plant Cell 10(8):1391–1406. https://doi.org/10.1105/tpc.10.8.1391
Liu C, Mao B, Ou S et al (2018) Correction to: OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 97(4–5):467–468. https://doi.org/10.1007/s11103-018-0745-6
Liu Y, Liu X, Wang X et al (2020) Heterologous expression of heat stress-responsive AtPLC9 confers heat tolerance in transgenic rice. BMC Plant Biol 20:514. https://doi.org/10.1186/s12870-020-02709-5
Lohia A, Hait NC, Majumder AL (1999) L-myo-inositol 1-phosphate synthase from Entamoeba histolytica. Mol Biochem Parasitol 98(1):67–79. https://doi.org/10.1016/s0166-6851(98)00147-9
Lüttge U, Popp M, Medina E, Cram WJ, Diaz M, Griffiths H (1989) Ecophysiol of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela: V. The batis maritime–Sesuvium portulacastrum vegetation unit. New Phytol 111(2):283–291. https://doi.org/10.1111/j.1469-8137.1989.tb00692.x
Ma L, Tian T, Lin R, Deng XW, Wang H, Li G (2016) Arabidopsis FHY3 and FAR1 regulate light-induced myo-inositol biosynthesis and oxidative stress responses by transcriptional activation of MIPS1. Mol Plant 9(4):541–557. https://doi.org/10.1016/j.molp.2015.12.013
Majee M, Maitra S, Ghosh Dastidar K et al (2004) A novel salt-tolerant L-myo-inositol 1- phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice: molecular cloning, bacterial overexpression, characterization and functional introgression into tobacco conferring salt-tolerance phenotype. J Biol Chem 279(27):28539–28552. https://doi.org/10.1074/jbc.m310138200
Majee M, Patra B, Mundree SG, Majumder AL (2005) Molecular cloning, bacterial overexpression and characterization L-myo-inositoL-1-phosphate synthase from a monocotyledonous resurrection plant, Xerophyta viscosa Baker. J Plant Biochem Biotech 14:95–99. https://doi.org/10.1007/BF03263235
Majumder AL, Duttagupta S, Goldwasser P, Donahue TF, Henry SA (1981) The mechanism of interallelic complementation at the INO1 locus in yeast: immunological analysis of mutants. Mol Gen Genet 184(3):347–354. https://doi.org/10.1007/BF00352503
Majumder AL, Johnson MD, Henry SA (1997) 1L-myo-inositol-1-phosphate synthase. Biochim Biophys Acta 1348(1–2):245–256. https://doi.org/10.1016/S0005-2760(97)00122-7
Majumder AL, Chatterjee A, Dastidar KG, Majee M (2003) Diversification and evolution of L-myo-inositol 1 phosphate synthase. FEBS Lett 533(1–2):3–10. https://doi.org/10.1016/S0014-5793(03)00974-8
McAdam SAM, Brodribb TJ (2012) Fern and lycophyte guard cells do not respond to endogenous abscisic acid. Plant Cell 24(4):1510–1521. https://doi.org/10.1105/tpc.112.096404
McCue LA, Thompson W, Carmack CS, Ryan MP, Liu JS, Derbyshire V, Lawrence CE (2001) Phylogenetic footprinting of transcription factor binding sites in proteobacterial genomes. Nucl Acids Res 29(3):774–782
Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S (2014) Abscisic acid and abiotic stress tolerance - different tiers of regulation. J Plant Physiol 171(7):486–496. https://doi.org/10.1016/j.jplph.2013.12.007
Meijer HJG, Berrie CP, Iurisci C, Divecha N, Musgrave A, Munnik T (2001) Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. Biochem J 360(Pt 2):491–498. https://doi.org/10.1042/0264-6021:3600491
Meng PH, Raynaud C, Tcherkez G et al (2009) Crosstalks between Myo-inositol metabolism, programmed cell death and basal immunity in Arabidopsis. PLoS ONE 4(10):e7364. https://doi.org/10.1371/journal.pone.0007364
Michell RH (2008) Inositol derivatives: evolution and functions. Nat Rev Mol Cell Biol 9:151–161. https://doi.org/10.1038/nrm2334
Mukherjee R, Mukherjee A, Bandyopadhyay S, Mukherjee S, Sengupta S, Ray S, Majumder AL (2019a) Selective manipulation of the inositol metabolic pathway for induction of salt-tolerance in indica rice variety. Sci Rep 9:5358. https://doi.org/10.1038/s41598-019-41809-7
Mukherjee S, Sengupta S, Mukherjee A, Basak P, Majumder AL (2019b) Abiotic stress regulates expression of galactinol synthase genes post-transcriptionally through intron retention in Rice. Planta 249(3):891–912. https://doi.org/10.1007/s00425-018-3046-z
Munir S, Mumtaz MA, Ahiakpa JK et al (2020) Genome-wide analysis of Myo-inositol oxygenase gene family in tomato reveals their involvement in ascorbic acid accumulation. BMC Genomics 21(1):284. https://doi.org/10.1186/s12864-020-6708-8
Munnik T (2014) PI-PLC: phosphoinositide-phospholipase C in plant signaling. In: Wang X (ed) Phospholipases in plant signaling: signaling and communication in plants. Springer, Berlin. https://doi.org/10.1007/978-3-642-42011-5_2
Murthy PPN (2006) Structure and nomenclature of inositol phosphates, phosphoinositides, and glycosylphosphatidylinositols. In: Majumder AL, Biswas BB (eds) Biology of inositols and phosphoinositides: subcellular biochemistry. Springer, Boston. https://doi.org/10.1007/0-387-27600-9_1
Nakashima K, Shinwari ZK, Sakuma Y et al (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration-and high-salinity-responsive gene expression. Plant Mol Biol 42(4):657–665. https://doi.org/10.1023/A:1006321900483
Nakashima K, Tran LS, Van Nguyen D et al (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51(4):617–630. https://doi.org/10.1111/j.1365-313X.2007.03168.x
Neelon K, Roberts MF, Stec B (2011) Crystal structure of a trapped catalytic intermediate suggests that forced atomic proximity drives the catalysis of mIPS. Biophys J 101(11):2816–2824
Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147(3):1251–1263. https://doi.org/10.1104/pp.108.122465
O’Malley RC, Huang SC, Song L et al (2016) Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165(5):1280–1292. https://doi.org/10.1016/j.cell.2016.04.038
Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schöffl F (2004) Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 136(2):3148–3158. https://doi.org/10.1104/pp.104.042606
Patra B, Dastidar KG, Maitra S, Bhattacharyya J, Majumder AL (2007) Functional identification of sll1383 from Synechocystis sp. PCC 6803 as L-myo-inositol 1-phosphate phosphatase (EC 3.1.3.25): molecular cloning expression and characterization. Planta 225(6):1547–1558. https://doi.org/10.1007/s00425-006-0441-7
Patra B, Ray S, Richter A, Majumder AL (2010) Enhanced salt tolerance of transgenic tobacco plants by co-expression of PcINO1 and McIMT1 is accompanied by increased level of myo-inositol and methylated inositol. Protoplasma 245(1–4):143–152. https://doi.org/10.1007/s00709-010-0163-3
Putney JW, Tomita T (2012) Phospholipase C signaling and calcium influx. Adv Biol Regul 52(1):152–164. https://doi.org/10.1016/j.advenzreg.2011.09.005
Rabbani MA, Maruyama K, Abe H et al (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133(4):1755–1767. https://doi.org/10.1104/pp.103.025742
Ray S, Patra B, Chatterjee AD, Ganguli A, Majumder AL (2010) Identification and organization of chloroplastic and cytosolic L-myo-inositol 1-phosphate synthase coding gene(s) in Oryza sativa: comparison with the wild halophytic rice. Porteresia Coarctata Planta 231(5):1211–1227. https://doi.org/10.1007/s00425-010-1127-8
RayChaudhuri A, Majumder AL (1996) Salinity-induced enhancement of L-myo-inositol 1-phosphate synthase in rice (Oryza sativa L.). Plant Cell Environ 19:1437–1442. https://doi.org/10.1111/j.1365-3040.1996.tb00023.x
RayChaudhuri A, Hait NC, Dasgupta S, Bhaduri TJ, Deb R, Majumder AL (1997) L-myo-inositol 1-phosphate synthase from plant sources: characteristics of the chloroplastic and cytosolic enzymes. Plant Physiol 115(2):727–736. https://doi.org/10.1104/pp.115.2.727
Redillas MC, Jeong JS, Kim YS et al (2012) The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J 10:792–805. https://doi.org/10.1111/j.1467-7652.2012.00697.x
Riikonen J, Kontunen-Soppela S, Ossipov V et al (2012) Needle metabolome, freezing tolerance and gas exchange in Norway spruce seedlings exposed to elevated temperature and ozone concentration. Tree Physiol 32(9):1102–1112. https://doi.org/10.1093/treephys/tps072
Sagar S, Biswas DK, Singh A (2020) Genomic and expression analysis indicate the involvement of phospholipase C family in abiotic stress signaling in chickpea (Cicer arietinum). Gene 753:144797. https://doi.org/10.1016/j.gene.2020.144797
Salehin M, Li B, Tang M et al (2019) Auxin-sensitive Aux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels. Nat Commun 10:4021. https://doi.org/10.1038/s41467-019-12002-1
Salvi P, Kamble NU, Majee M (2018) Stress inducible galactinol synthase of chickpea (CaGolS) implicates in heat and oxidative stress tolerance through reducing stress induced excessive reactive oxygen species accumulation. Plant Cell Physiol 59(1):155–166. https://doi.org/10.1093/pcp/pcx170
Sasaki K, Nagahashi G, Gretz MR, Taylor IE (1989) Use of per-C-deuterated myo-Inositol for study of cell wall synthesis in germinating beans. Plant Physiol 90(2):686–689. https://doi.org/10.1104/pp.90.2.686
Sengupta S, Patra B, Ray S, Majumder AL (2008) Inositol methyl transferase from a halophytic wild rice, Porteresia coarctata Roxb. (Tateoka): regulation of pinitol synthesis under abiotic stress. Plant Cell Environ 31(10):1442–1459. https://doi.org/10.1111/j.1365-3040.2008.01850.x
Sengupta S, Mukherjee S, Basak P, Majumder AL (2015) Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front Plant Sci 6(656):1–11. https://doi.org/10.3389/fpls.2015.00656
Sengupta S, Ray A, Mandal D, Chaudhuri RN (2020) ABI3 mediated repression of RAV1 gene expression promotes efficient dehydration stress response in Arabidopsis thaliana. Biochim Biophys Acta Gene Regul Mech 1863(9):194582. https://doi.org/10.1016/j.bbagrm.2020.194582
Shears SB (2018) Intimate connections: inositol pyrophosphates at the interface of metabolic regulation and cell signaling. J Cell Physiol 233(3):1897–1912. https://doi.org/10.1002/jcp.26017
Shim JS, Oh N, Chung PJ, Kim YS, Choi YD, Kim JK (2018) Overexpression of OsNAC14 improves drought tolerance in rice. Front Plant Sci 9:310. https://doi.org/10.3389/fpls.2018.00310
Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophysic Res Commun 250(1):161–170. https://doi.org/10.1006/bbrc.1998.9267
Singh A, Kanwar P, Pandey A et al (2013) Comprehensive genomic analysis and expression profiling of phospholipase C gene family during abiotic stresses and development in rice. PLoS ONE 8:e62494. https://doi.org/10.1371/journal.pone.0062494
Sullivan JL, Debusk AG (1973) Inositol-less death in Neurospora and cellular ageing. Nat New Biol 243(124):72–74
Sun Z, Qi X, Wang Z, Li P, Wu C, Zhang H, Zhao Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69:82–89. https://doi.org/10.1016/j.plaphy.2013.04.009
Taji T, Seki M, Yamaguchi-Shinozaki K, Kamada H, Giraudat J, Shinozaki K (1999) Mapping of 25 drought-inducible genes, RD and ERD in Arabidopsis thaliana. Plant Cell Physiol 40(1):119–123. https://doi.org/10.1093/oxfordjournals.pcp.a029469
Taji T, Ohsumi C, Iuchi S et al (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29(4):417–426. https://doi.org/10.1046/j.0960-7412.2001.01227.x
Takasaki H, Maruyama K, Kidokoro S et al (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284:173–183. https://doi.org/10.1007/s00438-010-0557-0
Takezawa D, Komatsu K, Sakata Y (2011) ABA in bryophytes: how a universal growth regulator in life became a plant hormone? J Plant Res 124:437–453. https://doi.org/10.1007/s10265-011-0410-5
Thomas MP, Mills SJ, Potter BV (2016) The “Other” inositols and their phosphates: synthesis, biology, and medicine (with recent advances in myo-inositol chemistry). Angew Chem Int Ed Engl 55(5):1614–1650. https://doi.org/10.1002/anie.201502227
Tietel Z, Wikoff WR, Kind T, Ma Y, Fiehn O (2020) Hyperosmotic stress in Chlamydomonas induces metabolomic changes in biosynthesis of complex lipids. Eur J Phycol 55(1):11–29. https://doi.org/10.1080/09670262.2019.1637547
Tran LS, Nakashima K, Sakuma Y et al (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498. https://doi.org/10.1105/tpc.104.022699
Tran LS, Nakashima K, Sakuma Y et al (2007) Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J 49(1):49–46. https://doi.org/10.1111/j.1365-313X.2006.02932.x
Tuteja N (2007) Abscisic acid and abiotic stress signalling. Plant Signal Behav 2(3):135–138. https://doi.org/10.4161/psb.2.3.4156
Ulaszewski S, Woodward JR, Cirillo VP (1978) Membrane damage associated with inositol-less death in Saccharomyces cerevisiae. J Bacteriol 136(1):49–54. https://doi.org/10.1128/JB.136.1.49-54.1978
Vernon DM, Bohnert HJ (1992) A novel methyl transferase induced by osmotic stress in the facultative halophyte Mesembryanthemum crystallinum. EMBO J 11(6):2077–2085
Wang H, Datla R, Georges F, Loewen M, Cutler AJ (1995) Promoters from kin1 and cor6.6, two homologous Arabidopsis thaliana genes: transcriptional regulation and gene expression induced by low temperature, ABA, osmoticum and dehydration. Plant Mol Biol 28:605–617. https://doi.org/10.1007/BF00021187
Wang WX, Vincour B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9(5):244–252. https://doi.org/10.1016/j.tplants.2004.03.006
Wang M, Li Z, Zhang Y et al (2021) An atlas of wheat epigenetic regulatory elements reveals subgenome-divergence in the regulation of development and stress responses. Plant Cell. https://doi.org/10.1093/plcell/koab028
Werner O, Espin RMR, Bopp M, Atzorn R (1991) Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186(1):99–103. https://doi.org/10.1007/BF00201503
Wu X, Kishitani S, Ito Y, Toriyama K (2009) Accumulation of raffinose in rice seedlings overexpressing OsWRKY11 in relation to desiccation tolerance. Plant Biotechnol 26:431–434. https://doi.org/10.5511/plantbiotechnology.26.431
Xu F, Park MR, Kitazumi A et al (2012) Cis-regulatory signatures of orthologous stress-associated bZIP transcription factors from rice, sorghum and Arabidopsis based on phylogenetic footprints. BMC Genomics 13:497. https://doi.org/10.1186/1471-2164-13-497
Xuan YH, Duan FY, Je BI et al (2017) Related to ABI3/VP1-Like 1 (RAVL1) regulates brassinosteroid-mediated activation of AMT1;2 in rice (Oryza sativa). J Exp Bot 68(3):727–737. https://doi.org/10.1093/jxb/erw442
Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Molec Gen Genet 236:331–340. https://doi.org/10.1007/BF00277130
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6(2):251–264. https://doi.org/10.1105/tpc.6.2.251
Yobi A, Wone BWM, Xu W et al (2013) Metabolomic Profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. Mol Plant 6(2):369–385. https://doi.org/10.1093/mp/sss155
Zhang Z, Gerstein M (2003) Of mice and men: phylogenetic footprinting aids the discovery of regulatory elements. J Biol 2:e11. https://doi.org/10.1186/1475-4924-2-11
Zhang Q, van Wijk R, Zarza X et al (2018) Knock-down of Arabidopsis PLC5 reduces primary root growth and secondary root formation while overexpression improves drought tolerance and causes stunted root hair growth. Plant Cell Physiol 59(10):2004–2019. https://doi.org/10.1093/pcp/pcy120
Zhang X, Long Y, Huang J, Xia J (2020) OsNAC45 is Involved in ABA response and salt tolerance in rice. Rice (n Y) 13(1):79. https://doi.org/10.1186/s12284-020-00440-1
Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun 379:985–989. https://doi.org/10.1016/j.bbrc.2008.12.163
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Zúñiga-González P, Zúñiga GE, Pizarro M et al (2016) Soluble carbohydrate content variation in Sanionia uncinata and Polytrichastrum alpinum, two Antarctic mosses with contrasting desiccation capacities. Biol Res 49:6. https://doi.org/10.1186/s40659-015-0058-z
Acknowledgements
ALM is currently an INSA Senior Scientist, while PB was supported by Institutional Research Associate fellowship
Funding
No specific funds were utilized for this work.
Author information
Authors and Affiliations
Contributions
ALM and PB conceptualized the idea primarily based on the previous work done in this laboratory and designed the outline of the review. PB conducted all the required supporting search, performed the bioinformatic analysis and wrote the draft manuscript. ALM reviewed and following thorough discussions finalized the same.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
13562_2021_708_MOESM1_ESM.tif
eFP data showing the genes with high inducibility under abiotic stresses- salt, drought and cold (retrieved from BAR databases for Arabidopsis and rice). Data for Arabidopsis were based on 0, 3, 6, 12 and 24 hrs of treatment for shoot and root, separately. Rice data available were of 3hrs post treatment (TIF 920 kb)
Rights and permissions
About this article
Cite this article
Basak, P., Majumder, A.L. Regulation of stress-induced inositol metabolism in plants: a phylogenetic search for conserved cis elements. J. Plant Biochem. Biotechnol. 30, 756–778 (2021). https://doi.org/10.1007/s13562-021-00708-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13562-021-00708-7