Regulation of sterol content and biosynthetic gene expression during flower opening and early fruit development in olive.
Journal
Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322
Informations de publication
Date de publication:
Dec 2019
Dec 2019
Historique:
received:
28
11
2018
revised:
21
03
2019
accepted:
25
03
2019
pubmed:
27
3
2019
medline:
10
3
2020
entrez:
27
3
2019
Statut:
ppublish
Résumé
Phytosterols are lipophilic membrane components essential not only for diverse cellular functions but also are biosynthetic precursors of the plant hormone, brassinosteroid (BR). However, the interaction between phytosterol and BR during early fleshy-fruit growth remains largely uncharacterized. In olive, phytosterols are important lipids because they affect oil quality, but phytosterol composition during flowering and early fruit development has not been explored. Here, we first investigated the temporal changes in phytosterol composition, and biosynthetic gene expression that occurred during olive flower opening and early fruit growth. Next, we analyzed the interrelationship between phytosterol and BR, whose levels we manipulated through the application of exogenous BRs (24-epibrassinolide, EBR) or a BR biosynthesis inhibitor (brassinazole, Brz). In this report, the profiling of phytosterol measurement revealed that β-sitosterol is the most abundant in olive reproductive organs. Our data demonstrate that both OeCYP51 and OeSMT2 genes are upregulated during floral anthesis in good agreement with the rise in cholesterol and β-sitosterol contents in olive flower. By contrast, the OeCYP51 and OeSMT2 genes displayed different expression patterns during early olive-fruit development. Furthermore, our data show that exogenous EBR enhanced the early olive-fruit growth, as well as the OeSMT2 transcript and β-sitosterol levels, but decreased the OeCYP51 transcript, squalene, campesterol and cholesterol levels, whereas the Brz treatment exerted the opposite effect. Overall, our findings indicate an up-regulation of β-sitosterol biosynthesis by BR at the transcriptional level during early olive-fruit growth, providing a valuable tool to unravel the physiological function of SMT2 in future studies.
Substances chimiques
Phytosterols
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
526-539Subventions
Organisme : Ministerio de Economía y Competitividad, Spain
ID : AGL2014-52194R
Informations de copyright
© 2019 Scandinavian Plant Physiology Society.
Références
Ajana H, el Antari A, Hafidi A (1998) Fatty acids and sterols evolution during the ripening of olives from the Moroccan Picholine cultivar. Grasas Aceites 49: 405-410
Alagna F, Mariotti R, Panara F, Caporali S, Urbani S, Veneziani G, Esposto S, Taticchi A, Rosati A, Rao R, Perrotta G, Servili M, Baldoni L (2012) Olive phenolic compounds: metabolic and transcriptional profiling during fruit development. BMC Plant Biol 2: 162
Alagna F, Cirilli M, Galla G, Carbone F, Daddiego L, Facella P, Lopez L, Colao C, Mariotti R, Cultrera N, Rossi M, Barcaccia G, Baldoni L, Muleo R, Perrotta G (2016) Transcript analysis and regulative events during flower development in olive (Olea europaea L.). PLoS ONE 11: e0152943. https://doi.org/10.1371/journal.pone.0152943
Asami T, Mizutani M, Fujioka S, Goda H, Min YK, Shimada Y, Nakano T, Takatsuto S, Matsuyama T, Nagata N, Sakata K, Yoshida S (2001) Selective interaction of triazole derivatives with DWF4, a cytochrome P450 monooxygenase of the brassinosteroid biosynthetic pathway, correlates with brassinosteroid deficiency in planta. J Biol Chem 276: 25687-25691
Aubert A, Marion J, Boulogne C, Bourge M, Abreu S, Bellec Y, Faure JD, Satiat-Jeunemaitre B (2011) Sphingolipids involvement in plant endomembrane differentiation: the BY2 case. Plant J 65: 958-971
Bak S, Kahn RA, Olsen CE, Halkier BA (1997) Cloning and expression in Escherichia coli of the obtusifoliol 14 alpha-demethylase of Sorghum bicolor (L.) Moench, a cytochrome P450 orthologous to the sterol 14 alpha-demethylases (CYP51) from fungi and mammals. Plant J 11: 191-201
Beck JG, Mathieu D, Loudet C, Buchoux S, Dufourc EJ (2007) Plant sterols in “rafts”: a better way to regulate membrane thermal shocks. FASEB J 21: 1714-1723
Benveniste P (2004) Biosynthesis and accumulation of sterols. Annu Rev Plant Biol 55: 429-457
Bloch KE (1983) Sterol structure and membrane function. CRC Crit Rev Biochem 14: 47-92
Boskou D (1996) Olive oil composition. In: Boskou D (ed) Olive Oil: Chemistry and Technology. AOCS Press, Champaign, pp 52-83
Boskou D (2015) Olive fruit, table olives, and olive oil bioactive constituents. In: Boskou D (ed) Olive and Olive Oil Bioactive Constituents. Elsevier, Chicago, IL, pp 1-30
Boutté Y, Grebe M (2009) Cellular processes relying on sterol function in plants. Curr Opin Plant Biol 12: 705-713
Bouvier-Navé P, Husselstein T, Desprez T, Benveniste P (1997) Identification of cDNAs encoding sterol methyl-transferases involved in the second methylation step of plant sterol biosynthesis. Eur J Biochem 246: 518-529
Bouvier-Navé P, Husselstein T, Benveniste P (1998) Two families of sterol methyltransferases are involved in the first and the second methylation steps of plant sterol biosynthesis. Eur J Biochem 256: 88-96
Burger C, Rondet S, Benveniste P, Schaller H (2003) Virus-induced silencing of sterol biosynthetic genes: identification of a Nicotiana tabacum L. obtusifoliol-14alpha-demethylase (CYP51) by genetic manipulation of the sterol biosynthetic pathway in Nicotiana benthamiana L. J Exp Bot 54: 1675-1683
Carland F, Fujioka S, Nelson T (2010) The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Plant Physiol 153: 741-756
Chalivendra SC, Lopez-Casado G, Kumar A, Kassenbrock AR, Royer S, Tovar-Mendez A, Covey PA, Dempsey LA, Randle AM, Stack SM, Rose JK, McClure B, Bedinger PA (2013) Developmental onset of reproductive barriers and associated proteome changes in stigma/styles of Solanum pennellii. J Exp Bot 64: 265-279
Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann KA (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J 26: 573-582
Clouse SD (2002) Arabidopsis mutants reveal multiple roles for sterols in plant development. Plant Cell 14: 1995-2000
Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49: 427-451
Conde C, Delrot S, Gero H (2008) Physiological, biochemical and molecular changes occurring during olive development and ripening. J Plant Physiol 165: 1545-1562
Corbacho J, Inês C, Paredes MA, Labrador J, Cordeiro AM, Gallardo M, Gomez-Jimenez MC (2018) Modulation of sphingolipid long-chain base composition and gene expression during early olive-fruit development, and putative role of brassinosteroid. J Plant Physiol 231C: 383-392
Diener AC, Li H, Zhou W, Whoriskey WJ, Nes WD, Fink GR (2000) Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell 12: 853-870
Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. N Biotechnol 26: 131-136
Fernández-Cuesta A, León L, Velasco L, De la Rosa R (2013) Changes in squalene and sterols associated with olive maturation. Food Res Int 54: 1885-1889
Ferrer A, Altabella T, Arro M, Boronat A (2017) Emerging roles for conjugated sterols in plants. Prog Lipid Res 67: 27-37
Foster LJ, de Hoog CL, Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 100: 5813-5818
Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ (2008) A role of brassinosteroids in early fruit development in cucumber. J Exp Bot 59: 2299-2308
Gil-Amado JA, Gomez-Jimenez MC (2013) Transcriptome analysis of mature fruit abscission control in olive. Plant Cell Physiol 54: 244-269. https://doi.org/10.1093/pcp/pcs179
Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130: 1319-1334
Gomez-Jimenez MC, Paredes MA, Gallardo M, Fernandez-Garcia N, Olmos E, Sanchez-Calle IM (2010) Tissue-specific expression of olive S-adenosyl methionine decarboxylase and spermidine synthase genes and polyamine metabolism during flower opening and early fruit development. Planta 232: 629-647
Gutiérrez F, Jiménez B, Ruíz A, Albi MA (1999) Effect of olive ripeness on the oxidative stability of virgin olive oil extracted from the varieties Picual and Hojiblanca and on the different components involved. J Agric Food Chem 47: 121-127
Hartmann MA (1998) Plant sterols and the membrane environment. Trends Plant Sci 3: 170-175
Hase Y, Fujioka S, Yoshida S, Sun G, Umeda M, Tanaka A (2005) Ectopic endoreduplication caused by sterol alteration results in serrated petals in Arabidopsis. J Exp Bot 56: 1263-1268
He JX, Fujioka S, Li TC, Kang SG, Seto H, Takatsuto S, Yoshida S, Jang JC (2003) Sterols regulate development and gene expression in Arabidopsis. Plant Physiol 131: 1258-1269
He WS, Zhu H, Chen ZY (2018) Plant sterols: chemical and enzymatic structural modifications and effects on their cholesterol-lowering activity. J Agric Food Chem 66: 3047-3062
Hobbs DH, Hume JH, Rolph CE, Cooke DT (1996) Changes in lipid composition during floral development of Brassica campestris. Phytochemistry 42: 335-339
Huang ZR, Lin YK, Fang JY (2009) Biological and pharmacological activities of squalene and related compounds: potential uses in cosmetic dermatology. Molecules 14: 540-554
Jang JC, Fujioka S, Tasaka M, Seto H, Takatsuto S, Ishii A, Aida M, Yoshida S, Sheen J (2000) A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev 14: 1485-1497
Kim HB, Schaller H, Goh CH, Kwon M, Choe S, An CS, Durst F, Feldmann KA, Feyereisen R (2005) Arabidopsis cyp51 mutant shows postembryonic seedling lethality associated with lack of membrane integrity. Plant Physiol 138: 2033-2047
Kim HB, Lee H, Oh CJ, Lee HY, Eum HL, Kim HS, Hong YP, Lee Y, Choe S, An CS, Choi SB (2010) Postembryonic seedling lethality in the steroldeficient Arabidopsis cyp51A2 mutant is partially mediated by the composite action of ethylene and reactive oxygen species. Plant Physiol 152: 192-205
Kushiro M, Nakano T, Sato K, Yamagishi K, Amasi T, Nakano A, Takatsuto S, Fujioka S, Ebizuka Y, Yoshida S (2001) Obtusifoliol 14α-demethylase (CYP51) antisense Arabidopsis shows slow growth and long life. Biochem Biophys Res Commun 285: 98-104
Kyçyk O, Aguilera MP, Gaforio JJ, Jiménez A, Beltrán G (2016) Sterol composition of virgin olive oil of forty-three olive cultivars from the World Collection Olive Germplasm Bank of Cordoba. J Sci Food Agric 96: 4143-4150
Lindsey K, Pullen ML, Topping JF (2003) Importance of plant sterols in pattern formation and hormone signalling. Trends Plant Sci 8: 521-525
Liu L, Jia C, Zhang M, Chen D, Chen S, Guo R, Guo D, Wang Q (2014) Ectopic expression of a BZR1-1D transcription factor in brassinosteroid signalling enhances carotenoid accumulation and fruit quality attributes in tomato. Plant Biotechnol J 12: 105-115
Luo M, Tan K, Xiao Z, Hu M, Liao P, Chen K (2008) Cloning and expression of two sterol C-24 methyltransferase genes from upland cotton (Gossypium hirsuturm L.). J Genet Genomics 35: 357-363
Madey E, Nowack LM, Thompson JE (2002) Isolation and characterization of lipid in phloem sap of canola. Planta 214: 625-634
Markham JE, Lynch DV, Napier JA, Dunn TM, Cahoon EB (2013) Plant sphingolipids: function follows form. Curr Opin Plant Biol 6: 350-357
Mathur J, Molnar G, Fujioka S, Takatsuto S, Sakurai A, Yokota T, Adam G, Voigt B, Nagy F, Maas C, Schell J, Koncz C, Szekeres M (1998) Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. Plant J 14: 593-602
Men S, Boutte Y, Ikeda Y, Li X, Palme K, Stierhof YD, Hartmann MA, Moritz T, Grebe M (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 10: 237-244
Mongrand S, Morel J, Laroche J, Claverol S, Carde JP, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ (2004) Lipid rafts in higher plant cells: purification and characterization of Triton X100 insoluble microdomains from tobacco plasma membrane. J Biol Chem 279: 36277-36286
Moreaua RA, Nyströmb L, Whitakerc BD, Winkler-Moserd JK, Baere DJ, Gebauerf SK, Hicksa KB (2018) Phytosterols and their derivatives: structural diversity, distribution, metabolism, analysis, and health-promoting uses. Prog Lipid Res 70: 35-61
Nakamura Y, Kobayashi K, Ohta H (2009) Activation of galactolipid biosynthesis in development of pistils and pollen tubes. Plant Physiol Biochem 47: 535-539
Neelakandan AK, Song Z, Wang J, Richards MH, Wub X, Valliyodan B, Nguyen HT, Nes WD (2009) Cloning, functional expression and phylogenetic analysis of plant sterol-24C-methyltransferases involved in sitosterol biosynthesis. Phytochemistry 70: 1982-1998
Neelakandan AK, Nguyen TM, Kumar R, Tran LS, Guttikonda SK, Quach TN, Aldrich DL, Nes WD, Nguyen HT (2010) Molecular characterization and functional analysis of Glycine max sterol methyl transferase 2 genes involved in plant membrane sterol biosynthesis. Plant Mol Biol 74: 503-518
Nelson DR, Schuler MA, Paquette SM, Werck-Reichhart D, Bak S (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol 135: 756-772
Nes WD, Song Z, Dennis AL, Zhou W, Nam J, Miller MB (2003) Biosynthesis of phytosterols. Kinetic mechanism for the enzymatic C-methylation of sterols. J Biol Chem 278: 34505-34516
Nie S, Huang S, Wang S, Cheng D, Liu J, Lv S, Li Q, Wang X (2017) Enhancing brassinosteroid signaling via overexpression of tomato (Solanum lycopersicum) SlBRI1 improves major agronomic traits. Front Plant Sci 10: 1386
Noguchi T, Fujioka S, Choe S, Takatsuto S, Tax FE, Yoshida S, Feldmann KA (2000) Biosynthetic pathways of brassinolide in Arabidopsis. Plant Physiol 124: 201-210
Nolan T, Chen J, Yin Y (2017) Cross-talk of Brassinosteroid signaling in controlling growth and stress responses. Biochem J 474: 2641-2661
Nomura T, Ueno M, Yamada Y, Takatsuto S, Takeuchi Y, Yokota T (2007) Roles of brassinosteroids and related mRNAs in pea seed growth and germination. Plant Physiol 143: 1680-1688
Owen RW, Mier W, Giacosa A, Hull WE, Spiegelhalder B, Bartsch H (2000) Phenolic compounds and squalene in olive oils: the concentration and antioxidant potential of total phenols, simple phenols, secoiridoids, lignans and squalene. Food Chem Toxicol 38: 647-659
Parra R, Paredes MA, Sanchez-Calle IM, Gomez-Jimenez MC (2013) Comparative transcriptional profiling analysis of olive ripe-fruit pericarp and abscission zone tissues shows expression differences and distinct patterns of transcriptional regulation. BMC Genomics 14: 866
Parra-Lobato MC, Paredes MA, Labrador J, Saucedo-García M, Gavilanes-Ruiz M, Gomez-Jimenez MC (2017) Localization of sphingolipid enriched plasma membrane regions and long-chain base composition during mature-fruit abscission in olive. Front Plant Sci 8: 1138
Peng L, Kawagoe Y, Hogan P, Delmer D (2002) Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295: 147-150
Pullen M, Clark N, Zarinkamar F, Topping J, Lindsey K (2010) Analysis of vascular development in the hydra sterol biosynthetic mutants of Arabidopsis. PLoS One 5: e12227
Ranalli A, Pollastri L, Contento S, Di Loreto G, Lannucci E, Lucera L, Russi F (2002) Sterol and alcohol components of seed, pulp and whole olive fruit oils: Their use to characterise olive fruit variety by multivariates. J Sci Food Agric 82: 854-859
Rugini E, De Pace C, Gutierrez-Pesce P, Muleo R (2011) Olea. In: Kole C (ed) Wild Crop Relatives: Genomic and Breeding Resources, Temperate Fruits. Springer-Verlag Berlin Heidelberg, Berlin
Schaeffer A, Bouvier-Nave P, Benveniste P, Schaller H (2000) Plant sterol-C24-methyl transferases: different profiles of tobacco transformed with SMT1 or SMT2. Lipids 35: 263-269
Schaeffer A, Bronner R, Benveniste P, Schaller H (2001) The ratio of campesterol to sitosterol that modulates growth in Arabidopsis is controlled by STEROL METHYLTRANSFERASE 2;1. Plant J 25: 605-615
Schaller H (2003) The role of sterols in plant growth and development. Prog Lipid Res 42: 163-175
Schaller H (2004) New aspects of sterol biosynthesis in growth and development of higher plants. Plant Physiol Biochem 42: 465-476
Schaller H, Bouvier-Nave P, Benveniste P (1998) Overexpression of an Arabidopsis cDNA encoding a sterol-C241-methyltransferase in tobacco modifies the ratio of 24-methyl cholesterol to sitosterol and is associated with growth reduction. Plant Physiol 118: 461-469
Schrick K, Mayer U, Horrichs A, Kuhnt C, Bellini C, Dangl J, Schmiddt J, Jurgens G (2000) FACKEL is a sterol C-14 reductase required for organized cell división and expansion in Arabidopsis embryogenesis. Genes Dev 14: 1471-1484
Schrick K, Mayer U, Martin G, Bellini C, Kuhnt C, Schmidt J, Jurgens G (2002) Interactions between sterol biosynthesis genes in embryonic development of Arabidopsis. Plant J 31: 61-73
Schrick K, Cordova C, Li G, Murray L, Fujiioka S (2011) A dynamic role for sterols in embryogenesis of Pisum sativum. Phytochemistry 72: 465-475
Schuler I, Milon A, Nakatani Y, Ourisson G, Albrecht AM, Benveniste P, Hartman MA (1991) Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers. Proc Natl Acad Sci U S A 88: 6926-6930
Serrano I, Suarez C, Olmedilla A, Rapoport HF, Rodriguez-Garcia MI (2008) Structural organization and cytochemical features of the pistil in olive (Olea europaea L.) cv. Picual at anthesis. Sex Plant Reprod 21: 99-111
Servili M, Sordini B, Esposto S, Urbani S, Veneziani G, Di Maio I, Selvaggini R, Taticchi A (2014) Biological activities of phenolic compounds of extra virgin olive oil. Antioxidants (Basel) 3: 1-23
Shi J, Gonzales RA, Bhattacharyya MK (1996) Identification and characterization of an S-adenosyl-L-methionine: delta 24-sterol C-methyltransferase cDNA from soybean. J Biol Chem 271: 9384-9389
Simon-Plas F, Perraki A, Bayer E, Gerbeau-Pissot P, Mongrand S (2011) An update on plant membrane rafts. Curr Opin Plant Biol 14: 642-649
Sitbon F, Jonsson L (2001) Sterol composition and growth of transgenic tobacco plants expressing type-1 and type-2 sterol methyltransferases. Planta 212: 568-572
Souter M, Topping J, Pullen M, Friml J, Palme K, Hackett R, Grierson D, Lindsey K (2002) Hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14: 1017-1031
Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138: 1117-1125
Tong H, Chu C (2018) Functional specificities of Brassinosteroid and potential utilization for crop improvement. Trends Plant Sci 23: 1016-1028
Valitova JN, Sulkarnayeva AG, Minibayeva FV (2016) Plant sterols: diversity, biosynthesis, and physiological functions. Biochemistry 81: 819-834
Vardhini BV, Rao SSR (2002) Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 61: 843-847
Vriet C, Russinova E, Reuzeau C (2013) From squalene to brassinolide: the steroid metabolic and signaling pathways across the plant kingdom. Mol Plant 6: 1738-1757
Vriet C, Lemmens K, Vandepoele K, Reuzeau C, Russinova E (2015) Evolutionary trails of plant steroid genes. Trends Plant Sci 20: 301-308
Willemsen V, Friml J, Grebe M, Van den Toorn A, Palme K, Scheres B (2003) Cell polarity and PIN protein positioning in Arabidopsis require sterol methyltransferase 1 function. Plant Cell 15: 612-625
Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen Z, Yu JQ (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230: 1185-1196
Yang H, Richter GL, Wang X, Młodzińska E, Carraro N, Ma G, Jenness M, Chao DY, Peer WA, Murphy AS (2013) Sterols and sphingolipids differentially function in trafficking of the Arabidopsis ABCB19 auxin transporter. Plant J 74: 37-47
Zhang C, Bai MY, Chong K (2014) Brassinosteroid-mediated regulation of agronomic traits in rice. Plant Cell Rep 33: 683-696