Novel allelic variation in the Phospholipase D alpha1 gene (OsPLDα1) of wild Oryza species implies to its low expression in rice bran.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 04 2020
20 04 2020
Historique:
received:
11
09
2018
accepted:
16
03
2020
entrez:
22
4
2020
pubmed:
22
4
2020
medline:
1
12
2020
Statut:
epublish
Résumé
Rice bran, a by-product after milling, is a rich source of phytonutrients like oryzanols, tocopherols, tocotrienols, phytosterols, and dietary fibers. Moreover, exceptional properties of the rice bran oil make it unparalleled to other vegetable oils. However, a lipolytic enzyme Phospholipase D alpha1 (OsPLDα1) causes rancidity and 'stale flavor' in the oil, and thus limits the rice bran usage for human consumption. To improve the rice bran quality, sequence based allele mining at OsPLDα1 locus (3.6 Kb) was performed across 48 accessions representing 11 wild Oryza species, 8 accessions of African cultivated rice, and 7 Oryza sativa cultivars. From comparative sequence analysis, 216 SNPs and 30 InDels were detected at the OsPLDα1 locus. Phylogenetic analysis revealed 20 OsPLDα1 cDNA variants which further translated into 12 protein variants. The O. officinalis protein variant, when compared to Nipponbare, showed maximum variability comprising 22 amino acid substitutions and absence of two peptides and two β-sheets. Further, expression profiling indicated significant differences in transcript abundance within as well as between the OsPLDα1 variants. Also, a new OsPLDα1 transcript variant having third exon missing in it, Os01t0172400-06, has been revealed. An O. officinalis accession (IRGC101152) had lowest gene expression which suggests the presence of novel allele, named as OsPLDα1-1a (GenBank accession no. MF966931). The identified novel allele could be further deployed in the breeding programs to overcome rice bran rancidity in elite cultivars.
Identifiants
pubmed: 32313086
doi: 10.1038/s41598-020-62649-w
pii: 10.1038/s41598-020-62649-w
pmc: PMC7170842
doi:
Substances chimiques
DNA, Complementary
0
Dietary Fiber
0
Phospholipase D
EC 3.1.4.4
Rice Bran Oil
LZO6K1506A
Tocopherols
R0ZB2556P8
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6571Références
Hargrove, K. L. Processing and utilization of rice bran in the United States. Rice Science and Technology. Marshall, W. E. and Wadsworth, J. I. (Eds.). New York: Marcel Dekker Inc. (1994).
Hu, W., Wells, J. H., Shin, T. S. & Godber, J. S. Comparison of isopropanol and hexane for extraction of vitamin E and oryzanols from stabilized rice bran. J. Am. Oil Chem. Soci. 73, 1653–1656 (1996).
doi: 10.1007/BF02517967
Saunders, R. M. The properties of rice bran as a foodstuff. Cereal Foods World 35, 632–636 (1990).
Yoshino, G. Effects of γ-oryzanol on hyperlipidemic subjects. Current Therapy Res. 45, 543–552 (1989).
Krishna, A. G. G., Khatoon, S. & Babylatha, R. Frying performance of processed rice bran oils. J. Food Lipids 12, 1–11 (2005).
doi: 10.1111/j.1745-4522.2005.00001.x
Nicolosi, R. J., Ausman, L. M. & Hegsted, D. M. Rice bran oil lowers serum total and low density lipoprotein cholesterol and apo B levels in nonhuman primates. Atherosclerosis 88, 133–142 (1991).
pubmed: 1892480
doi: 10.1016/0021-9150(91)90075-E
pmcid: 1892480
Salunkhe, D. K., Chavan, J. K., Adsule, R. N. & Kadam, S. S. Rice in World oilseeds: Chemistry, technology, and utilization. New York: Van Nostrand Reinhold. pp. 424–428 (1992).
Takano, K., Kamoi, I. & Obara, T. Changes in lipid components and lipolytic enzyme activities of rice bran during storage (Studies on the mechanisms of lipids-hydrolysing in rice bran part I). J. Jpn. Soc. Food Sci. Technol. 33, 310–315 (1986).
doi: 10.3136/nskkk1962.33.5_310
Barnes, P. and Galliard, T. Rancidity in cereal products. Lipid Technol. 3, 23–28 (1991).
List, G. R., Mounts, T. L. & Lanser, A. C. Factors promoting the formation of nonhydratable soybean phosphatides. J. Am. Oil Chem. Soc. 69, 403–410 (1992).
doi: 10.1007/BF02540945
Nakayama, Y., Saio, K. & Kito, M. Decomposition of phospholipids in soybean during storage. Cereal Chem. 58, 260–264 (1981).
Takano, K., Kamoi, I. & Obara, T. Purification and properties of rice bran phospholipase D. J. Jpn. Soc. Food Sci. Technol. 34, 8–13 (1987).
doi: 10.3136/nskkk1962.34.8
Takano, K., Kamoi, I. & Obara, T. Properties and degradation of rice bran spherosome. J. Jpn. Soc. Food Sci. Technol. 36, 468–474 (1989).
doi: 10.3136/nskkk1962.36.6_468
Suzuki, Y. et al. Volatile components in stored rice [Oryza sativa (L.)] of varieties with and without lipoxygenase-3 in seeds. J. Agric. Food Chem. 47, 1119–1124 (1999).
pubmed: 10552425
doi: 10.1021/jf980967a
pmcid: 10552425
Zhou, Z., Robards, K., Helliwell, S. & Blanchard, C. Ageing of stored rice: Changes in chemical and physical attributes. J. Cereal Sci. 35, 65–78 (2002).
doi: 10.1006/jcrs.2001.0418
Gang, L., Fang, L. & Hong-Wei, X. Genome-wide analysis of the phospholipase D family in Oryza sativa and functional characterization of PLDβ1 in seed germination. Cell Res. 17, 881–894 (2007).
doi: 10.1038/cr.2007.77
Qin, C. & Wang, X. The Arabidopsis phospholipase D family: characterization of a Ca
pubmed: 11891260
pmcid: 152217
doi: 10.1104/pp.010928
Ueki, J., Morioka, S., Komari, T. & Kumashiro, T. Purification and characterization of phospholipase D (PLD) from rice (Oryza sativa L.) and cloning of cDNA for PLD from rice and maize (Zea mays L.). Plant Cell Physiol. 36, 903–914 (1995).
pubmed: 7551587
doi: 10.1093/oxfordjournals.pcp.a078837
pmcid: 7551587
Suzuki, Y., Takeuchi, Y. & Shirasawa, K. Identification of a seed phospholipase D null allele in rice (Oryza sativa L.) and development of SNP markers for phospholipase D deficiency. Crop Sci. 51, 2113–2118 (2011).
doi: 10.2135/cropsci2010.12.0716
Sato, Y. et al. RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res. 39, 1141–1148 (2011).
doi: 10.1093/nar/gkq1085
Suzuki, Y. Isolation and characterization of a rice (Oryza sativa L.) mutant deficient in seed phospholipase D, an enzyme involved in the degradation of oil-body membranes. Crop Sci. 51, 567–573 (2011).
doi: 10.2135/cropsci2010.08.0460
Ramezanzadeh, F. M., Rao, R. M., Windhauser, M., Prinyawiwatkul, W. & Marshall, W. E. Prevention of hydrolytic rancidity in rice bran during storage. J. Agric. Food Chem. 47, 2997–3000 (1999).
pubmed: 10552599
doi: 10.1021/jf981168v
pmcid: 10552599
Malekian, F. et al. In: Lipase and lipoxygenase activity, functionality, and nutrient losses in rice bran during storage: Bull 870. Louisiana Agric Exp Stn: LSU Agric Cent, Baton Rouge, LA. pp 1–56 (2000).
McCaskill, D. R. & Zhang, F. Use of rice bran oil in foods. Food Technol. 53, 50–53 (1999).
Doebley, J. F., Gaut, B. S. & Smith, B. D. The molecular genetics of crop domestication. Cell 127, 1309–1321 (2006).
doi: 10.1016/j.cell.2006.12.006
Khush, G. S. & Ling, K. C. Inheritance of resistance to grassy stunt virus and its vector in rice. J. Hered. 65, 135–136 (1974).
doi: 10.1093/oxfordjournals.jhered.a108483
Amante-Bordeos, A. et al. Transfer of bacterial blight and blast resistance from the tetraploid wild rice Oryza minuta to cultivated rice (Oryza sativa). Theor. Appl. Genet. 84, 345–354 (2002).
Amarawathi, Y. et al. Mapping of quantitative trait loci for basmati quality traits in rice (Oryza sativa L.). Mol. Breed. 21, 49–65 (2008).
doi: 10.1007/s11032-007-9108-8
Saitoh, K., Onishi, K., Mikami, I., Thidar, K. & Sano, Y. Allelic diversification at the C (OsC1) locus of wild and cultivated rice: nucleotide changes associated with phenotypes. Genetics 168, 997–1007 (2004).
pubmed: 15514070
pmcid: 1448844
doi: 10.1534/genetics.103.018390
Wang, X., Jia, Y., Shu, Q. Y. & Wu, D. Haplotype diversity at the Pi-ta locus in cultivated rice and its wild relatives. Phytopath. 98, 1305–1311 (2008).
doi: 10.1094/PHYTO-98-12-1305
Yang, S. et al. Genetic variation of NBS-LRR class resistance genes in rice lines. Theor. Appl. Genet. 116, 165–177 (2008).
pubmed: 17932646
doi: 10.1007/s00122-007-0656-4
pmcid: 17932646
Yoshida, K. & Miyashita, N. T. Nucleotide polymorphism in the Adh2 region of the wild rice Oryza rufipogon. Theor. Appl. Genet. 111, 1215–1228 (2005).
pubmed: 16133310
doi: 10.1007/s00122-005-0054-8
pmcid: 16133310
Mikami, I. et al. Allelic diversification at the wx locus in landraces of Asian rice. Theor. Appl. Genet. 116, 979–989 (2008).
pubmed: 18305920
doi: 10.1007/s00122-008-0729-z
pmcid: 18305920
Brooks, S. A., Yan, W., Jackson, A. K. & Deren, C. W. A natural mutation in rc reverts white rice pericarp to red and results in a new, dominant, wild-type allele: Rc-g. Theor. Appl. Genet. 117, 575–580 (2008).
pubmed: 18516586
doi: 10.1007/s00122-008-0801-8
pmcid: 18516586
Leiros, I., Secundo, F., Zambonelli, C., Servi, S. & Edward, H. The first crystal structure of a phospholipase D. Structure 8, 655–667 (2000).
pubmed: 10873862
doi: 10.1016/S0969-2126(00)00150-7
pmcid: 10873862
Kumar, G. R. et al. Allele mining in Crops: prospects and potentials. Biotechnol. Adv. 28, 451–461 (2010).
pubmed: 20188810
doi: 10.1016/j.biotechadv.2010.02.007
pmcid: 20188810
Zhao, Q. et al. Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nature genetics 50, 278–284 (2018).
pubmed: 29335547
doi: 10.1038/s41588-018-0041-z
pmcid: 29335547
Sweeny, M. & McCouch, S. The complex history of the domestication of rice. Ann. Bot. 100, 951–957 (2007).
doi: 10.1093/aob/mcm128
Second, G. Origin of the genic diversity of cultivated rice growing environment in West Africa. (Oryza spp.): Study of the polymorphism scored at 40 isozyme loci. Japanese. Journal of Genetics 57, 25–57 (1982).
Semon, M., Nielsen, R., Jones, M. P. & McCouch, S. R. The population structure of African cultivated rice Oryza glaberrima (Steud.): evidence for elevated levels of linkage disequilibrium caused by admixture with O. sativa and ecological adaptation. Genetics 169, 1639–1647 (2005).
pubmed: 15545652
pmcid: 1449534
doi: 10.1534/genetics.104.033175
Meyer, R. S. et al. Domestication history and geographical adaptation inferred from a SNP map of African rice. Nature Genetics; https://doi.org/10.1038/ng.3633 (2016).
Wang, M. et al. The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nature genetics 46, 982–988 (2014).
pubmed: 25064006
pmcid: 7036042
doi: 10.1038/ng.3044
Sang, T. & Ge, S. Understanding rice domestication and implications for cultivar improvement. Curr. Opin. Plant. Biol. 16, 139–146 (2013).
pubmed: 23545218
doi: 10.1016/j.pbi.2013.03.003
pmcid: 23545218
Vaughan, D. A., Lu, B. R. & Tomooka, N. The evolving story of rice evolution. Plant Sci. 174, 394–408 (2008).
doi: 10.1016/j.plantsci.2008.01.016
Banaticla‐Hilario, M. C. N., van den Berg, R. G., Hamilton, N. R. S. & McNally, K. L. Local differentiation amidst extensive allele sharing in Oryza nivara and O. rufipogon. Ecology and Evolution 3, 3047–3062 (2013).
pubmed: 24101993
pmcid: 3790550
doi: 10.1002/ece3.689
Morishima, H. Evolution and domestication of rice. Rice Genetics IV, IRRI. pp 63–78 (2001).
Zheng, X. M. & Ge, S. Ecological divergence in the presence of gene flow in two closely related Oryza species (Oryza rufipogon and O. nivara). Mol. Ecol. 19, 2439–2454 (2010).
pubmed: 20653085
doi: 10.1111/j.1365-294X.2010.04674.x
pmcid: 20653085
Barbier, P., Morishima, H. & Ishiharna, A. Phylogenetic relationship of annual and perennial wild rice: probing by direct DNA sequencing. Theor. Appl. Genet. 81, 693–702 (1991).
pubmed: 24221388
doi: 10.1007/BF00226739
pmcid: 24221388
Lu, B. R., Zheng, K. L. & Qian, H. R. Genetic differentiation of wild relatives of rice as assessed by RFLP analysis. Theor. Appl. Genet. 106, 101–106 (2002).
pubmed: 12582876
doi: 10.1007/s00122-002-1013-2
pmcid: 12582876
Zhu, Q. & Ge, S. Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol. 167, 249–265 (2005).
pubmed: 15948847
doi: 10.1111/j.1469-8137.2005.01406.x
pmcid: 15948847
Zhu, Q., Zheng, X., Luo, J., Gaut, B. S. & Ge, S. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol. Biol. Evol. 24, 875–888 (2007).
pubmed: 17218640
doi: 10.1093/molbev/msm005
pmcid: 17218640
Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501 (2012).
pubmed: 23034647
doi: 10.1038/nature11532
pmcid: 23034647
Liu, R., Zheng, X. M., Zhou, L. & Zhou, H. F. nd Ge, S. Population genetic structure of Oryza rufipogon and Oryza nivara: implications for the origin of O. nivara. Mol. Ecol. 24, 5211–5228 (2015).
pubmed: 26340227
doi: 10.1111/mec.13375
pmcid: 26340227
Samal, R. et al. Morphological and molecular dissection of wild rices from eastern India suggests distinct speciation between O. rufipogon and O. nivara populations. Scientific reports 8, 1–13 (2018).
doi: 10.1038/s41598-017-17765-5
Melaku, G. et al. Genetic diversity and differentiation of the African wild rice (Oryza longistaminata chev. et roehr) in Ethiopia. Scientific African; https://doi.org/10.1016/j.sciaf.2019.e00138 (2019).
Zhang, Y. et al. Genome and comparative transcriptomics of African wild rice Oryza longistaminata provide insights into molecular mechanism of rhizomatousness and self-incompatibility. Molecular plant 8, 1683–1686 (2015).
pubmed: 26358679
doi: 10.1016/j.molp.2015.08.006
pmcid: 26358679
He, R. et al. A systems-wide comparison of red rice (Oryza longistaminata) tissues identifies rhizome specific genes and proteins that are targets for cultivated rice improvement. BMC Plant Biology 14, 46 (2014).
pubmed: 24521476
pmcid: 3933257
doi: 10.1186/1471-2229-14-46
Reuscher, S. et al. Assembling the genome of the African wild rice Oryza longistaminata by exploiting synteny in closely related Oryza species. Commun, Biol., https://doi.org/10.1038/s42003-018-0171-y (2018).
Ren, F., Lu, B. R., Li, S., Huang, J. & Zhu, Y. A. comparative study of genetic relationships among the AA-genome Oryza species using RAPD and SSR markers. Theor. Appl. Genet. 108, 113–120 (2003).
pubmed: 14504744
doi: 10.1007/s00122-003-1414-x
pmcid: 14504744
Iwamoto, M., Nagashima, H., Nagamine, T., Higo, H. & Higo, K. p-SINE1-like intron of the CatA catalase homologs and phylogenetic relationships among AA-genome Oryza and related species. Theor. Appl. Genet. 98, 853–861 (1999).
doi: 10.1007/s001220051144
Cheng, C., Tsuchimoto, S., Ohtsubo, H. & Ohtsubo, E. Evolutionary relationships among rice species with AA genome based on SINE insertion analysis. Genes Genet. Syst. 77, 323–334 (2002).
pubmed: 12441643
doi: 10.1266/ggs.77.323
pmcid: 12441643
Wambugu, P. W., Brozynska, M., Furtado, A., Waters, D. L. & Henry, R. J. Relationships of wild and domesticated rices (Oryza AA genome species) based upon whole chloroplast genome sequences. Scientific Reports 5, 13957, https://doi.org/10.1038/srep13957 (2015).
doi: 10.1038/srep13957
pubmed: 26355750
pmcid: 4564799
Cynthia, C. V., Linda, L. S. & Kenneth, M. O. Long-term balancing selection at the Phosphorus Starvation Tolerance 1 (PSTOL1) locus in wild, domesticated and weedy rice (Oryza). BMC Plant Biol. 16, 101, https://doi.org/10.1186/s12870-016-0783-7 (2016).
doi: 10.1186/s12870-016-0783-7
Gao, L. Z. et al. Evolution of Oryza chloroplast genomes promoted adaptation to diverse ecological habitats. Commun. Boil. 2, 1–13 (2019).
doi: 10.1038/s42003-018-0242-0
Bao, Y. & Ge, S. Origin and phylogeny of Oryza species with the CD genome based on multiple‐gene sequence data. Plant Syst. Evol. 249, 55–66 (2004).
doi: 10.1007/s00606-004-0173-8
Wang, B. et al. Polyploid evolution in Oryza officinalis complex of the genus Oryza. BMC Evol. Biol. 9, 250, https://doi.org/10.1186/1471-2148-9-250 (2009).
doi: 10.1186/1471-2148-9-250
pubmed: 19828030
pmcid: 2770061
Li, C., Zhang, D., Ge, S., Lu, B. & Hong, D. Differentiation and inter‐genomic relationships among C, E and D genomes in the Oryza officinalis complex (Poaceae) as revealed by multicolor genomic in situ hybridization. Theor. Appl. Genet. 103, 197–203 (2001).
doi: 10.1007/s001220100562
Guo, Y. L. & Ge, S. Molecular phylogeny of Oryzeae (Poaceae) based on DNA sequences from chloroplast, mitochondrial, and nuclear genomes. Am. J. Bot. 92, 1548–1558 (2005).
pubmed: 21646172
doi: 10.3732/ajb.92.9.1548
pmcid: 21646172
Hirsch, C. D., Wu, Y., Yan, H. & Jiang, J. Lineage‐specific adaptive evolution of the centromeric protein CENH3 in diploid and allotetraploid Oryza species. Mol. Biol. Evol. 26, 2877–2885 (2009).
pubmed: 19741004
doi: 10.1093/molbev/msp208
pmcid: 19741004
Kumari, A. et al. Mining of rice blast resistance gene Pi54 shows effect of single nucleotide polymorphisms on phenotypic expression of the alleles. Eur. J. Pl. Pathol. 137, 55–65 (2013).
doi: 10.1007/s10658-013-0216-5
Li, H. J., Li, X. H., Xiao, J. H., Wing, R. A. & Wang, S. P. Ortholog alleles at Xa3/Xa26 locus confer conserved race-specific resistance against Xanthomonas oryzae in rice. Molecular Plant 5, 281–290 (2012).
pubmed: 21930802
doi: 10.1093/mp/ssr079
pmcid: 21930802
Hammond, S. M. et al. Human ADP-ribosylation factor-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J. Biol. Chem. 270, 29640–29643 (1995).
pubmed: 8530346
doi: 10.1074/jbc.270.50.29640
pmcid: 8530346
Sung, T. et al. Mutagenesis of phospholipase D defines a superfamily including a trans-Golgi viral protein required for poxvirus pathogenicity. EMBO J. 16, 4519–4530 (1997).
pubmed: 9303296
pmcid: 1170078
doi: 10.1093/emboj/16.15.4519
Isshiki, M. et al. A naturally occuring funcional allele of the rice waxy locus has a GT to TT mutation at the 5′splice site of the first intron. Plant J. 15, 133–138 (1998).
pubmed: 9744101
doi: 10.1046/j.1365-313X.1998.00189.x
pmcid: 9744101
Nalefski, E. A. & Falke, J. J. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 5, 2375–2390 (1996).
pubmed: 8976547
pmcid: 2143302
doi: 10.1002/pro.5560051201
Perisic, O., Fong, S., Lynch, D. E., Bycroft, M. & Williams, R. L. Crystal structures of a calcium-phospholipid binding domain from cytosolic phospholipase A2. J. Biol. Chem. 273, 1596–1604 (1998).
pubmed: 9430701
doi: 10.1074/jbc.273.3.1596
pmcid: 9430701
Pappan, K. & Wang, X. Plant phospholipase Dα is an acidic phospholipase active at near-physiological Ca
pubmed: 10441386
doi: 10.1006/abbi.1999.1325
pmcid: 10441386
Liscovitch, M., Czarny, M., Fiucci, G. & Tang, X. Phospholipase D: molecular and cell biology of a novel gene family. Biochem. J. 345, 401–415 (2000).
pubmed: 10642495
pmcid: 1220771
doi: 10.1042/bj3450401
Ponting, C. P. & Perker, P. J. Extending the C2 domain family: C2s in PKCs delta, epsilon, eta, theta, phospholipases, GAPs, and perforin. Protein Sci. 5, 162–166 (1996).
pubmed: 8771209
pmcid: 2143250
doi: 10.1002/pro.5560050120
Ryu, S. B. & Wang, X. Activation of phospholipase D and the possible mechanism of activation in wound-induced lipid hydrolysis in castor bean leaves. Biochimica et. Biophysica Acta. 1303, 243–250.
Zheng, L., Krishnamoorthi, R., Zolkiewski, M. & Wang, X. Distinct Ca
pubmed: 10777500
doi: 10.1074/jbc.M001945200
pmcid: 10777500
Croessmann, S. et al. PIK3CA C2 domain deletions hyperactivate phosphoinositide 3-kinase (PI3K), generate oncogene dependence, and are exquisitely sensitive to PI3Kα inhibitors. Clinical Cancer Research 24, 1426–1435 (2018).
pubmed: 29284706
doi: 10.1158/1078-0432.CCR-17-2141
pmcid: 29284706
McGee, J. D. et al. Rice phospholipase D isoforms show differential cellular location and gene induction. Plant Cell Physiol. 44, 1013–1026 (2003).
pubmed: 14581626
doi: 10.1093/pcp/pcg125
pmcid: 14581626
Janecek, S., Svensson, B. & Henrissat, B. Domain evolution in the α-amylase family. J. Mol. Evol. 45, 322–331 (1997).
pubmed: 9302327
doi: 10.1007/PL00006236
pmcid: 9302327
MacGregor, E. A. α-Amylase structure and activity. J. Protein Chem. 7, 399–415 (1988).
pubmed: 3267138
doi: 10.1007/BF01024888
pmcid: 3267138
Ponting, C. P. & Kerr, I. D. A novel family of phospholipase D homologues that include phospholipid synthases and putative endonucleases: identification of duplicated repeats and potential active site residues. Protein Sci. 5, 914–922 (1996).
pubmed: 8732763
pmcid: 2143407
doi: 10.1002/pro.5560050513
Arhab, Y., Abousalham, A. & Noiriel, A. Plant phospholipase D mining unravels new conserved residues important for catalytic activity. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids 1864, 688–703 (2019).
Zheng, L., Shan, J., Krishnamoorthi, R. & Wang, X. Activation of plant phospholipase Dα by phosphatidylinositol 4, 5-bisphosphate: characterization of binding site and mode of action. Biochemistry 41, 4546–4553 (2002).
pubmed: 11926815
doi: 10.1021/bi0158775
pmcid: 11926815
Higashibata, A. et al. Decreased expression of myogenic transcription factors and myosin heavy chains in Caenorhabditis elegans muscles developed during space flight. J. Exp. Biol. 209, 3209–3218 (2006).
pubmed: 16888068
doi: 10.1242/jeb.02365
pmcid: 16888068
Woods, D. C., Alvarez, C. & Johnson, A. L. Cisplatin-mediated sensitivity to TRAIL-induced cell death in human granulosa tumor cells. Gynecol. Oncol. 108, 632–640 (2008).
pubmed: 18191995
doi: 10.1016/j.ygyno.2007.11.034
pmcid: 18191995
Paik, S. et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817–2826 (2004).
pubmed: 15591335
doi: 10.1056/NEJMoa041588
pmcid: 15591335
Larsson, P. K. A., Claesson, H. E. & Kennedy, B. P. Multiple Splice Variants of the Human Calcium-independent Phospholipase A
pubmed: 9417066
doi: 10.1074/jbc.273.1.207
pmcid: 9417066
Campbell, M. A., Haas, B. J., Hamilton, J. P., Mount, S. M. & Buell, C. R. Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC genomics 7, 327 (2006).
pubmed: 17194304
pmcid: 1769492
doi: 10.1186/1471-2164-7-327
Liu, J. et al. Alternative splicing of rice WRKY62 and WRKY76 transcription factor genes in pathogen defense. Plant Physiology 171, 1427–1442 (2016).
pubmed: 27208272
pmcid: 4902586
Ta, K. N. et al. Differences in meristem size and expression of branching genes are associated with variation in panicle phenotype in wild and domesticated African rice. EvoDevo; https://doi.org/10.1186/s13227-017-0065-y (2017).
Saghai-Maroof, M. A., Soliman, K. M., Jorgensen, R. A. & Allard, R. W. Ribosomal DNA spacer length polymorphism in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc. Nat. Acad. Sci., USA 81, 8014–8019 (1984).
doi: 10.1073/pnas.81.24.8014
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
pubmed: 17846036
doi: 10.1093/bioinformatics/btm404
pmcid: 17846036
Sali, A. & Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815 (1993).
pubmed: 8254673
doi: 10.1006/jmbi.1993.1626
pmcid: 8254673
Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
pmcid: 15264254
Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).
pubmed: 27004904
doi: 10.1093/molbev/msw054
pmcid: 27004904
Kaur, A. et al. Novel cis-acting regulatory elements in wild Oryza species impart improved rice bran quality by lowering the expression of Phospholipase D alpha1 enzyme (OsPLDα1). Mol. Biol. Rep. 47, 401–422 (2019).
pubmed: 31642040
doi: 10.1007/s11033-019-05144-4
pmcid: 31642040
Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C
pubmed: 18546601
doi: 10.1038/nprot.2008.73
pmcid: 18546601