Genome-wide survey and expression analysis of the putative non-specific lipid transfer proteins in Brassica rapa L

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Li, Jun ^a   Gao, Guizhen ^a   Xu, Kun ^a   Chen, Biyun ^a   Yan, Guixin ^a   Li, Feng ^a   Qiao, Jiangwei ^a   Zhang, Tianyao ^a   Wu, Xiaoming ^a  

^a AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID TRANSFER PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BRASSICA RAPA; BRNSLTP 1 GENE; BRNSLTP 11 GENE; BRNSLTP 2 GENE; BRNSLTP 3 GENE; BRNSLTP 4 GENE; BRNSLTP 5 GENE; BRNSLTP 6 GENE; BRNSLTP 8 GENE; BRNSLTP 9 GENE; BRNSLTP GENE; CHROMOSOMAL LOCALIZATION; DISULFIDE BOND; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; INTRON; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT LEAF; PLANT REPRODUCTION; PLANT ROOT;

AMINO ACID SEQUENCE; BASE SEQUENCE; BRASSICA RAPA; CARRIER PROTEINS; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION, PLANT; GENETIC VARIATION; GENOME, PLANT; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PLANT PROTEINS; PROTEIN CONFORMATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84900334273     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084556     Document Type: Article

References (102)

1. Blein JP, Coutos-Thevenot P, Marion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7: 293-296. (Pubitemid 36726512)
2. Sleight RG (1987) Intracellular lipid transport in eukaryotes. Annu Rev Physiol 49: 193-208.
3. Sprong H, van der Sluijs P, van Meer G (2001) How proteins move lipids and lipids move proteins. Nat Rev Mol Cell Biol 2: 504-513. (Pubitemid 33673400)
4. Kaplan MR, Simoni RD (1985) Intracellular transport of phosphatidylcholine to the plasma membrane. J Cell Biol 101: 441-445. (Pubitemid 15239119)
5. Vance JE, Aasman EJ, Szarka R (1991) Brefeldin A does not inhibit the movement of phosphatidylethanolamine from its sites for synthesis to the cell surface. J Biol Chem 266: 8241-8247. (Pubitemid 21906503)
6. Holthuis JC, Levine TP (2005) Lipid traffic: floppy drives and a superhighway. Nat Rev Mol Cell Biol 6: 209-220. (Pubitemid 40314922)
7. Levine T (2004) Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol 14: 483-490.
8. Kader JC (1975) Proteins and the intracellular exchange of lipids. I. Stimulation of phospholipid exchange between mitochondria and microsomal fractions by proteins isolated from potato tuber. Biochim Biophys Acta 380: 31-44.
9. Ostergaard J, Vergnolle C, Schoentgen F, Kader JC (1993) Acyl-binding/lipid-transfer proteins from rape seedlings, a novel category of proteins interacting with lipids. Biochim Biophys Acta 1170: 109-117. (Pubitemid 23308221)
10. Kader JC, Julienne M, Vergnolle C (1984) Purification and characterization of a spinach-leaf protein capable of transferring phospholipids from liposomes to mitochondria or chloroplasts. Eur J Biochem 139: 411-416.
11. Arondel V, Vergnolle C, Tchang F, Kader JC (1990) Bifunctional lipid-transfer: fatty acid-binding proteins in plants. Mol Cell Biochem 98: 49-56. (Pubitemid 20309215)
12. Tsuboi S, Osafune T, Tsugeki R, Nishimura M, Yamada M (1992) Nonspecific lipid transfer protein in castor bean cotyledon cells: subcellular localization and a possible role in lipid metabolism. J Biochem 111: 500-508.
13. Jose-Estanyol M, Gomis-Ruth FX, Puigdomenech P (2004) The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiol Biochem 42: 355-365. (Pubitemid 38800983)
14. Douliez JP, Michon T, Elmorjani K, Marion D (2000) Structure, biological and technological functions of lipid transfer proteins and indolines, the major lipid binding proteins from cereal kernels. J Cereal Sci 32: 1-20. (Pubitemid 30613389)
15. Vergnolle C, Arondel V, Jolliot A, Kader JC (1992) Phospholipid transfer proteins from higher plants. Methods Enzymol 209: 522-530.
16. Shin DH, Lee JY, Hwang KY, Kim KK, Suh SW (1995) High-resolution crystal structure of the non-specific lipid-transfer protein from maize seedlings. Structure 3: 189-199.
17. Boutrot F, Chantret N, Gautier MF (2008) Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics 9: 86.
18. Liu W, Huang D, Liu K, Hu S, Yu J, et al. (2010) Discovery, Identification and Comparative Analysis of Non-Specific Lipid Transfer Protein (nsLtp) Family in Solanaceae. Genomics, Proteomics & Bioinformatics 8: 229-237.
19. Kader JC (1996) Lipid-Transfer Proteins in Plants. Annu Rev Plant Physiol Plant Mol Biol 47: 627-654.
20. Carvalho Ade O, Gomes VM (2007) Role of plant lipid transfer proteins in plant cell physiology-a concise review. Peptides 28: 1144-1153.
21. Kim TH, Park JH, Kim MC, Cho SH (2008) Cutin monomer induces expression of the rice OsLTP5 lipid transfer protein gene. J Plant Physiol 165: 345-349.
22. Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140: 176-183. (Pubitemid 43956313)
23. Lee SB, Go YS, Bae HJ, Park JH, Cho SH, et al. (2009) Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol 150: 42-54.
24. Sterk P, Booij H, Schellekens GA, Van Kammen A, De Vries SC (1991) Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3: 907-921. (Pubitemid 21913752)
25. Coutos-Thevenot P, Jouenne T, Maes O, Guerbette F, Grosbois M, et al. (1993) Four 9-kDa proteins excreted by somatic embryos of grapevine are isoforms of lipid-transfer proteins. Eur J Biochem 217: 885-889. (Pubitemid 23326869)
26. Potocka I, Baldwin TC, Kurczynska EU (2012) Distribution of lipid transfer protein 1 (LTP1) epitopes associated with morphogenic events during somatic embryogenesis of Arabidopsis thaliana. Plant Cell Rep 31: 2031-2045.
27. Chen C, Chen G, Hao X, Cao B, Chen Q, et al. (2011) CaMF2, an anther-specific lipid transfer protein (LTP) gene, affects pollen development in Capsicum annuum L. Plant Sci 181: 439-448.
28. Zhang D, Liang W, Yin C, Zong J, Gu F, et al. (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154: 149-162.
29. Park SY, Jauh GY, Mollet JC, Eckard KJ, Nothnagel EA, et al. (2000) A lipid transfer-like protein is necessary for lily pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12: 151-164.
30. Park SY, Lord EM (2003) Expression studies of SCA in lily and confirmation of its role in pollen tube adhesion. Plant Mol Biol 51: 183-189.
31. Chae K, Gonong BJ, Kim SC, Kieslich CA, Morikis D, et al. (2010) A multifaceted study of stigma/style cysteine-rich adhesin (SCA)-like Arabidopsis lipid transfer proteins (LTPs) suggests diversified roles for these LTPs in plant growth and reproduction. J Exp Bot 61: 4277-4290.
32. Chae K, Kieslich CA, Morikis D, Kim SC, Lord EM (2009) A gain-of-function mutation of Arabidopsis lipid transfer protein 5 disturbs pollen tube tip growth and fertilization. Plant Cell 21: 3902-3914.
33. Chae K, Lord EM (2011) Pollen tube growth and guidance: roles of small, secreted proteins. Ann Bot 108: 627-636.
34. Nieuwland J, Feron R, Huisman BA, Fasolino A, Hilbers CW, et al. (2005) Lipid transfer proteins enhance cell wall extension in tobacco. Plant Cell 17: 2009-2019.
35. Guiderdoni E, Cordero MJ, Vignols F, Garcia-Garrido JM, Lescot M, et al. (2002) Inducibility by pathogen attack and developmental regulation of the rice Ltp1 gene. Plant Mol Biol 49: 683-699. (Pubitemid 34609177)
36. Jung HW, Kim W, Hwang BK (2003) Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses. Plant Cell Environ 26: 915-928. (Pubitemid 36737998)
37. Lin P, Xia L, Ng TB (2007) First isolation of an antifungal lipid transfer peptide from seeds of a Brassica species. Peptides 28: 1514-1519. (Pubitemid 47247959)
38. Sarowar S, Kim YJ, Kim KD, Hwang BK, Ok SH, et al. (2009) Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep 28: 419-427.
39. Pii Y, Molesini B, Pandolfini T (2013) The involvement of Medicago truncatula non-specific lipid transfer protein N5 in the control of rhizobial infection. Plant Signal Behav 8.
40. Sels J, Mathys J, De Coninck BM, Cammue BP, De Bolle MF (2008) Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem 46: 941-950.
41. Schweiger W, Steiner B, Ametz C, Siegwart G, Wiesenberger G, et al. (2013) Transcriptomic characterization of two major Fusarium resistance quantitative trait loci (QTLs), Fhb1 and Qfhs.ifa-5A, identifies novel candidate genes. Mol Plant Pathol 14: 772-785.
42. Guo C, Ge X, Ma H (2013) The rice OsDIL gene plays a role in drought tolerance at vegetative and reproductive stages. Plant Mol Biol 82: 239-253.
43. Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64: 1755-1767.
44. Giordani T, Buti M, Natali L, Pugliesi C, Cattonaro F, et al. (2011) An analysis of sequence variability in eight genes putatively involved in drought response in sunflower (Helianthus annuus L.). Theor Appl Genet 122: 1039-1049.
45. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419: 399-403.
46. Pii Y, Pandolfini T, Crimi M (2010) Signaling LTPs: A new plant LTPs sub-family? Plant Signal Behav 5.
47. Thoma S, Hecht U, Kippers A, Botella J, De Vries S, et al. (1994) Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiol 105: 35-45.
48. Wang NJ, Lee CC, Cheng CS, Lo WC, Yang YF, et al. (2012) Construction and analysis of a plant non-specific lipid transfer protein database (nsLTPDB). BMC Genomics 13 Suppl 1: S9.
49. Jose-Estanyol M, Puigdomenech P (2000) Plant cell wall glycoproteins and their genes. Plant Physiology and Biochemistry 38: 97-108. (Pubitemid 30170277)
50. Dvorakova L, Cvrckova F, Fischer L (2007) Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genomics 8: 412.
51. Edstam MM, Viitanen L, Salminen TA, Edqvist J (2011) Evolutionary history of the non-specific lipid transfer proteins. Mol Plant 4: 947-964.
52. Wang HW, Hwang SG, Karuppanapandian T, Liu A, Kim W, et al. (2012) Insight into the molecular evolution of non-specific lipid transfer proteins via comparative analysis between rice and sorghum. DNA Res 19: 179-194.
53. Lehmann MS, Pebay-Peyroula E, Cohen-Addad C, Odani S (1989) Crystallographic data for soybean hydrophobic protein. J Mol Biol 210: 235-236. (Pubitemid 19286600)
54. Tassin S, Broekaert WF, Marion D, Acland DP, Ptak M, et al. (1998) Solution structure of Ace-AMP1, a potent antimicrobial protein extracted from onion seeds. Structural analogies with plant nonspecific lipid transfer proteins. Biochemistry 37: 3623-3637. (Pubitemid 28162917)
55. Long M, Rosenberg C, Gilbert W (1995) Intron phase correlations and the evolution of the intron/exon structure of genes. Proc Natl Acad Sci U S A 92: 12495-12499. (Pubitemid 26014096)
56. Wang X, Wang H, Wang J, Sun R, Wu J, et al. (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43: 1035-1039.
57. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4: 10.
58. Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37: 859-869. (Pubitemid 28329442)
59. Rogers HJ, Bate N, Combe J, Sullivan J, Sweetman J, et al. (2001) Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 45: 577-585. (Pubitemid 32515951)
60. Champigny MJ, Shearer H, Mohammad A, Haines K, Neumann M, et al. (2011) Localization of DIR1 at the tissue, cellular and subcellular levels during Systemic Acquired Resistance in Arabidopsis using DIR1:GUS and DIR1:EGFP reporters. BMC Plant Biol 11: 125.
61. Champigny MJ, Isaacs M, Carella P, Faubert J, Fobert PR, et al. (2013) Long distance movement of DIR1 and investigation of the role of DIR1-like during systemic acquired resistance in Arabidopsis. Front Plant Sci 4: 230.
62. Cardoza V, Stewart CN (2004) Invited review: Brassica biotechnology: Progress in cellular and molecular biology. In Vitro Cellular & Developmental Biology-Plant 40: 542-551.
63. Cheng F, Mandakova T, Wu J, Xie Q, Lysak MA, et al. (2013) Deciphering the diploid ancestral genome of the Mesohexaploid Brassica rapa. Plant Cell 25: 1541-1554.
64. U N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7: 389-452.
65. Parkin IA, Sharpe AG, Keith DJ, Lydiate DJ (1995) Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38: 1122-1131. (Pubitemid 3015089)
66. Bohuon EJ, Keith DJ, Parkin IA, Sharpe AG, Lydiate DJ (1996) Alignment of the conserved C genomes of Brassica oleracea and Brassica napus. Theor Appl Genet 93: 833-839.
67. Panjabi P, Jagannath A, Bisht NC, Padmaja KL, Sharma S, et al. (2008) Comparative mapping of Brassica juncea and Arabidopsis thaliana using Intron Polymorphism (IP) markers: homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes. BMC Genomics 9: 113.
68. Suwabe K, Morgan C, Bancroft I (2008) Integration of Brassica A genome genetic linkage map between Brassica napus and B. rapa. Genome 51: 169-176. (Pubitemid 351573622)
69. Lukens L, Zou F, Lydiate D, Parkin I, Osborn T (2003) Comparison of a Brassica oleracea genetic map with the genome of Arabidopsis thaliana. Genetics 164: 359-372. (Pubitemid 36617719)
70. Parkin IA, Sharpe AG, Lydiate DJ (2003) Patterns of genome duplication within the Brassica napus genome. Genome 46: 291-303. (Pubitemid 36610682)
71. Parkin IA, Gulden SM, Sharpe AG, Lukens L, Trick M, et al. (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171: 765-781. (Pubitemid 43158406)
72. Lim GA, Jewell EG, Li X, Erwin TA, Love C, et al. (2007) A comparative map viewer integrating genetic maps for Brassica and Arabidopsis. BMC Plant Biol 7: 40.
73. Lysak MA, Koch MA, Pecinka A, Schubert I (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res 15: 516-525. (Pubitemid 41065010)
74. Lysak MA, Cheung K, Kitschke M, Bures P (2007) Ancestral chromosomal blocks are triplicated in Brassiceae species with varying chromosome number and genome size. Plant Physiol 145: 402-410. (Pubitemid 47575139)
75. Tapia G, Morales-Quintana L, Parra C, Berbel A, Alcorta M (2013) Study of nsLTPs in Lotus japonicus genome reveal a specific epidermal cell member (LjLTP10) regulated by drought stress in aerial organs with a putative role in cutin formation. Plant Mol Biol 82: 485-501.
76. Evans DE, Taylor PE, Singh MB, Knox RB (1992) The interrelationship between the accumulation of lipids, protein and the level of acyl carrier protein during the development of Brassica napus L. Planta 186: 343-354.
77. Piffanelli P, Ross JH, Murphy DJ (1997) Intra- and extracellular lipid composition and associated gene expression patterns during pollen development in Brassica napus. Plant J 11: 549-562. (Pubitemid 27158960)
78. Zhou Z, Dun X, Xia S, Shi D, Qin M, et al. (2012) BnMs3 is required for tapetal differentiation and degradation, microspore separation, and pollen-wall biosynthesis in Brassica napus. J Exp Bot 63: 2041-2058.
79. Boavida LC, Becker JD, Feijo JA (2005) The making of gametes in higher plants. Int J Dev Biol 49: 595-614. (Pubitemid 41615613)
80. Foster GD, Robinson SW, Blundell RP, Roberts MR, Hodge R (1992) A Brassica napus mRNA encoding a protein homologous to phospholipid transfer proteins, is expressed especially in the tapetum and developing microspores. Plant Sci 84: 184-192.
81. Park HC, Kim ML, Kang YH, Jeon JM, Yoo JH, et al. (2004) Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol 135: 2150-2161.
82. Ellerstrom M, Stalberg K, Ezcurra I, Rask L (1996) Functional dissection of a napin gene promoter: identification of promoter elements required for embryo and endosperm-specific transcription. Plant Mol Biol 32: 1019-1027. (Pubitemid 27049899)
83. Stalberg K, Ellerstom M, Ezcurra I, Ablov S, Rask L (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199: 515-519. (Pubitemid 26350738)
84. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, et al. (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34: D247-251.
85. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
86. Eisenhaber B, Wildpaner M, Schultz CJ, Borner GH, Dupree P, et al. (2003) Glycosylphosphatidylinositol lipid anchoring of plant proteins. Sensitive prediction from sequence- and genome-wide studies for Arabidopsis and rice. Plant Physiol 133: 1691-1701. (Pubitemid 38047300)
87. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-36.
88. Alam N, Gourinath S, Dey S, Srinivasan A, Singh TP (2001) Substrate-inhibitor interactions in the kinetics of alpha-amylase inhibition by ragi alpha-amylase/trypsin inhibitor (RATI) and its various N-terminal fragments. Biochemistry 40: 4229-4233. (Pubitemid 32319569)
89. Guerche P, Tire C, De Sa FG, De Clercq A, Van Montagu M, et al. (1990) Differential Expression of the Arabidopsis 2S Albumin Genes and the Effect of Increasing Gene Family Size. Plant Cell 2: 469-478. (Pubitemid 120029605)
90. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
91. Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29: 1023-1026.
92. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
93. Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11: 535-542. (Pubitemid 44740519)
94. Yuan J, Chen D, Ren Y, Zhang X, Zhao J (2008) Characteristic and expression analysis of a metallothionein gene, OsMT2b, down-regulated by cytokinin suggests functions in root development and seed embryo germination of rice. Plant Physiol 146: 1637-1650. (Pubitemid 352844064)
95. Wang Z, Xie W, Chi F, Li C (2005) Identification of non-specific lipid transfer protein-1 as a calmodulin-binding protein in Arabidopsis. FEBS Lett 579: 1683-1687. (Pubitemid 40341543)
96. Brotman Y, Lisec J, Meret M, Chet I,Willmitzer L, et al. (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158: 139-146.
97. Molina A, Garcia-Olmedo F (1997) Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J 12: 669-675. (Pubitemid 27434045)
98. Molina A, Diaz I, Vasil IK, Carbonero P, Garcia-Olmedo F (1996) Two cold-inducible genes encoding lipid transfer protein LTP4 from barley show differential responses to bacterial pathogens. Mol Gen Genet 252: 162-168.
99. Tian A, Cao J, Huang L, Yu X, Ye W (2009) Characterization of a male sterile related gene BcMF15 from Brassica campestris ssp. chinensis. Mol Biol Rep 36: 307-314.
100. Wang C, Xie W, Chi F, Hu W, Mao G, et al. (2008) BcLTP, a novel lipid transfer protein in Brassica chinensis, may secrete and combine extracellular CaM. Plant Cell Rep 27: 159-169.
101. Sawano Y, Hatano K, Miyakawa T, Komagata H, Miyauchi Y, et al. (2008) Proteinase inhibitor from ginkgo seeds is a member of the plant nonspecific lipid transfer protein gene family. Plant Physiol 146: 1909-1919. (Pubitemid 352844057)
102. Choi YE, Lim S, Kim HJ, Han JY, Lee MH, et al. (2012) Tobacco NtLTP1, a glandular-specific lipid transfer protein, is required for lipid secretion from glandular trichomes. Plant J 70: 480-491.