Skip to main content
Log in

Overview of Alternaria alternata Membrane Proteins

  • Review article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Alternaria species are mainly saprophytic fungi, but some pathotypes of Alternaria alternata infect economically important plants including cereal crops, vegetables and fruits. Specially, A. alternata generates toxins which contaminate food and feed. To date, management of A. alternata relies primarily on fungicides. However, the control efficacy in most cases is below expectation due to ubiquity of A. alternata and resistance to fungicides. To mitigate resistance and develop long-lasting fungicides, uncovering multiple rather than single target is a prerequisite. Membrane proteins are potential targets of fungicides owing to wide participation in myriad biochemical events especially material transport, signal transduction and pathogenicity. However, so far, little is known about the distribution and molecular structure of A. alternata membrane proteins (AAMPs). Herein we summarize AAMPs by data mining and subsequent structure prediction. We also outline the state-of-the-art research advances of AAMPs especially those closely related to pathogenicity. Overall, this review aims to portray a picture of AAMPs and provide valuable insights for future development of highly efficient fungicides towards A. alternata or beyond.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Thomma BP (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236. https://doi.org/10.1046/J.1364-3703.2003.00173.X

    Article  CAS  PubMed  Google Scholar 

  2. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H (2013) Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37:44–46. https://doi.org/10.1111/j.1574-6976.2012.00350.x

    Article  CAS  PubMed  Google Scholar 

  3. Cho Y (2015) How the necrotrophic fungus Alternaria brassicicola kills plant cells remains an enigma. Eukaryot Cell 14:335–344. https://doi.org/10.1128/EC.00226-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kan J, Liu T, Ma N, Li H, Li X, Wang J, Zhang B, Chang Y, Lin J (2017) Transcriptome analysis of Callery pear (Pyrus calleryana) reveals a comprehensive signaling network in response to Alternaria alternata. PLoS ONE 12:e0184988. https://doi.org/10.1371/journal.pone.0184988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sudharshana TN, Venkatesh HN, Nayana B, Manjunath K, Mohana DC (2018) Anti-microbial and anti-mycotoxigenic activities of endophytic Alternaria alternata isolated from Catharanthus roseus (L.) G. Don.: molecular characterisation and bioactive compound isolation. Mycology 10:40–48. https://doi.org/10.1080/21501203.2018.1541933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Yang LN, He MH, Ouyang HB, Zhu W, Pan ZC, Sui QJ, Shang LP, Zhan J (2019) Cross-resistance of the pathogenic fungus Alternaria alternata to fungicides with different modes of action. BMC Microbiol 19:205. https://doi.org/10.1186/s12866-019-1574-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Yu PL, Chen LH, Chung KR (2016) How the pathogenic fungus Alternaria alternata copes with stress via the response regulators SSK1 and SHO1. PLoS ONE 11:e0149153. https://doi.org/10.1371/journal.pone.0149153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Yamagishi D, Otani H, Kodama M (2006) G protein signaling mediates developmental processes and pathogenesis of Alternaria alternata. Mol Plant Microbe Interact 19:1280–1288. https://doi.org/10.1094/MPMI-19-1280

    Article  CAS  PubMed  Google Scholar 

  9. Chen S, Kim C, Lee JM, Lee HA, Fei Z, Wang L, Apel K (2015) Blocking the QB-binding site of photosystem II by tenuazonic acid, a non-host-specific toxin of Alternaria alternata, activates singlet oxygen-mediated and EXECUTER-dependent signalling in Arabidopsis. Plant Cell Environ 38:1069–1080. https://doi.org/10.1111/pce.12462

    Article  CAS  PubMed  Google Scholar 

  10. Caille O, Rossier C, Perron K (2007) A copper-activated two-component system interacts with zinc and imipenem resistance in Pseudomonas aeruginosa. J Bacteriol 189:4561–4568. https://doi.org/10.1128/JB.00095-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Moore J, Bailey SES, Benmechernene Z, Tzitzilonis C, Griffiths NJE, Virji M, Derrick JP (2005) Recognition of saccharides by the OpcA, OpaD, and OpaB outer membrane proteins from Neisseria meningitidis. J Biol Chem 280:31489–31497. https://doi.org/10.1074/jbc.M506354200

    Article  CAS  PubMed  Google Scholar 

  12. Roelants FM, Leskoske KL, Martinez MM, Locke MN, Thorner J (2017) The TORC2-dependent signaling network in the yeast Saccharomyces cerevisiae. Biomolecules 7:66. https://doi.org/10.3390/biom7030066

    Article  CAS  PubMed Central  Google Scholar 

  13. Singh R, Capalash N, Sharma P (2017) Immunoprotective potential of BamA, the outer membrane protein assembly factor, against MDR Acinetobacter baumannii. Sci Rep 7:12411. https://doi.org/10.1038/s41598-017-12789-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Singh R, Garg N, Shukla G, Capalash N, Sharma P (2016) Immunoprotective efficacy of Acinetobacter baumannii outer membrane protein, FilF, predicted in silico as a potential vaccine candidate. Front Microbiol 7:158. https://doi.org/10.3389/fmicb.2016.00158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Garg N, Singh R, Shukla G, Capalash N, Sharma P (2016) Immunoprotective potential of in silico predicted Acinetobacter baumannii outer membrane nuclease NucAb. Int J Med Microbiol 306:1–9. https://doi.org/10.1016/j.ijmm.2015.10.005

    Article  CAS  PubMed  Google Scholar 

  16. Singh R, Garg N, Capalash N, Kumar R, Kumar M, Sharma P (2014) In silico analysis of Acinetobacter baumannii outer membrane protein BamA as a potential immunogen. Int J Pure Appl Sci Technol 21:32–39

    CAS  Google Scholar 

  17. Chluba-De TJ, De TM, Jaggin V, Eberle AN (1997) Cloning of a human multispanning membrane protein cDNA: evidence for a new protein family. Gene 197:195–204. https://doi.org/10.1016/S0378-1119(97)00263-1

    Article  Google Scholar 

  18. Sivadon P, Peypouquet MF, Doignon F, Aigle M, Crouzet M (1997) Cloning of the multicopy suppressor gene SUR7: evidence for a functional relationship between the yeast actin-binding protein Rvs167 and a putative membranous protein. Yeast 13:747–761. https://doi.org/10.1002/(SICI)1097-0061(19970630)13:8%3c747:AID-YEA137%3e3.0.CO;2-L

    Article  CAS  PubMed  Google Scholar 

  19. Denison SH, Negrete-Urtasun S, Mingot JM, Tilburn J, Mayer WA, Goel A, Espeso EA, Penalva MA, Arst HN Jr (1998) Putative membrane components of signal transduction pathways for ambient PH regulation in Aspergillus and meiosis in Saccharomyces are homologous. Mol Microbiol 39:259–264. https://doi.org/10.1046/j.1365-2958.1998.01058.x

    Article  Google Scholar 

  20. Young ME, Karpova TS, Brügger B, Moschenross DM, Wang GK, Schneiter R, Wieland FT, Cooper JA (2002) The Sur7p family defines novel cortical domains in Saccharomyces cerevisiae, affects sphingolipid metabolism, and is involved in sporulation. Mol Cell Biol 22:927–934. https://doi.org/10.1128/MCB.22.3.927-934.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C, Walter P (2006) Eisosomes mark static sites of endocytosis. Nature 439:998–1003. https://doi.org/10.1038/nature04472

    Article  CAS  PubMed  Google Scholar 

  22. Amerik AY, Hochstrasser M (2004) Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta 1695:189–207. https://doi.org/10.1016/j.bbamcr.2004.10.003

    Article  CAS  PubMed  Google Scholar 

  23. Archibald JM, Teh EM, Keeling PJ (2003) Novel ubiquitin fusion proteins: ribosomal protein P1 and actin. J Mol Biol 328:771–778. https://doi.org/10.1016/S0022-2836(03)00374-7

    Article  CAS  PubMed  Google Scholar 

  24. Knipscheer P, van Dijk WJ, Olsen JV, Mann M, Sixma TK (2007) Noncovalent interaction between Ubc9 and SUMO promotes SUMO chain formation. EMBO J 26:2797–2807. https://doi.org/10.1038/sj.emboj.7601711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Jack DL, Yang NM, Saier MH (2001) The drug/metabolite transporter superfamily. Eur J Biochem 268:3620–3639. https://doi.org/10.1046/j.1432-1327.2001.02265.x

    Article  CAS  PubMed  Google Scholar 

  26. Lou HB, Chen M, Black SS, Bushell SR, Ceccarelli M, Mach T, Beis K, Low AS, Bamford VA, Booth IR (2011) Altered antibiotic transport in OmpC mutants isolated from a series of clinical strains of multi-drug resistant E. coli. PLoS ONE 6:e25825. https://doi.org/10.1371/journal.pone.0025825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Gristwood T, Mcneil MB, Clulow JS, Salmond GPC, Fineran PC (2011) Pigs and PigP regulate prodigiosin biosynthesis in Serratia via differential control of divergent operons, which include predicted transporters of sulfur-containing molecules. J Bacteriol 193:1076–1085. https://doi.org/10.1128/JB.00352-10

    Article  CAS  PubMed  Google Scholar 

  28. Ote T, Hashimoto M, Ikeuchi Y, Suetsugu M, Suzuki T, Katayama T, Kato J (2006) Involvement of the Escherichia coli folate-binding protein YgfZ in RNA modification and regulation of chromosomal replication initiation. Mol Microbiol 60:252. https://doi.org/10.1111/j.1365-2958.2006.05067.x

    Article  CAS  Google Scholar 

  29. Wang DS, Shaw R, Winkelmann JC, Shaw G (1994) Binding of PH domains of β-adrenergic-receptor kinase and β-spectrin to WD40/β-transducin repeat containing regions of the β-subunit of trimeric G-proteins. Biochem Biophys Res Commun 203:29–35. https://doi.org/10.1006/bbrc.1994.2144

    Article  CAS  PubMed  Google Scholar 

  30. Yao L, Kawakami Y, Kawakami T (1994) The pleckstrin homology domain of Bruton tyrosine kinase interacts with protein kinase C. Proc Natl Acad Sci USA 91:9175–9179. https://doi.org/10.1073/pnas.91.19.9175

    Article  CAS  PubMed  Google Scholar 

  31. Doerks T, Strauss M, Brendel M, Bork P (2000) GRAM, a novel domain in glucosyltransferases, myotubularins and other putative membrane-associated proteins. Trends Biochem Sci 25:483–485. https://doi.org/10.1016/S0968-0004(00)01664-9

    Article  CAS  PubMed  Google Scholar 

  32. Begley MJ, Taylor GS, Kim SA, Veine DM, Dixon JE, Stuckey JA (2003) Crystal structure of a phosphoinositide phosphatase, MTMR2: insights into myotubular myopathy and Charcot-Marie-Tooth syndrome. Mol Cell 12:1391–1402. https://doi.org/10.1016/S1097-2765(03)00486-6

    Article  CAS  PubMed  Google Scholar 

  33. Graham TR (2004) Membrane targeting: getting arl to the golgi. Curr Biol 14:483–485. https://doi.org/10.1016/j.cub.2004.06.017

    Article  CAS  Google Scholar 

  34. Liu YW, Lee SW, Lee FJS (2006) Arl1p is involved in transport of the GPI-anchored protein Gas1p from the late Golgi to the plasma membrane. J Cell Sci 119:3845–3855. https://doi.org/10.1242/jcs.03148

    Article  CAS  PubMed  Google Scholar 

  35. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A (2003) The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J Biol Chem 278:34739–34742. https://doi.org/10.1074/jbc.C300269200

    Article  CAS  PubMed  Google Scholar 

  36. Kumar P, Wolberger C (2015) Structure of the yeast Bre1 RING domain. Proteins Struct Funct Bioinf 83:1185–1190. https://doi.org/10.1002/prot.24812

    Article  CAS  Google Scholar 

  37. Okuyama E, Yamamoto R, Ichikawa Y, Tsubaki M (1998) Structural basis for the electron transfer across the chromaffin vesicle membranes catalyzed by cytochrome b561: analyses of cDNA nucleotide sequences and visible absorption spectra. Biochem Biophys Acta 1383:269–278. https://doi.org/10.1016/S0167-4838(97)00216-1

    Article  CAS  PubMed  Google Scholar 

  38. Fleming PJ, Kent UM (1987) Secretory vesicle cytochrome b561: a transmembrane electron transporter. Ann NY Acad Sci 493:101–107. https://doi.org/10.1111/j.1749-6632.1987.tb27187.x

    Article  CAS  PubMed  Google Scholar 

  39. Stefan CP, Zhang N, Sokabe T, Rivetta A, Slayman CL, Montell C, Cunningham KW (2013) Activation of an essential calcium signaling pathway in Saccharomyces cerevisiae by Kch1 and Kch2, putative low-affinity potassium transporters. Eukaryot Cell 12:204–214. https://doi.org/10.1128/EC.00299-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Trott A, Morano KA (2004) SYM1 is the stress-induced Saccharomyces cerevisiae ortholog of the mammalian kidney disease gene Mpv17 and is required for ethanol metabolism and tolerance during heat shock. Eukaryot Cell 3:620–631. https://doi.org/10.1128/EC.3.3.620-631.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lai MH, Bard M, Pierson CA, Alexander JF, Goebl M, Carter GT, Kirsch DR (1994) The identification of a gene family in the Saccharomyces cerevisiae ergosterol biosynthesis pathway. Gene 140:41–49

    Article  CAS  Google Scholar 

  42. Mitchell AG, Martin CE (1997) Fah1p, a Saccharomyces cerevisiae cytochrome b5 fusion protein, and its Arabidopsis thaliana homolog that lacks the cytochrome b5 domain both function in the alpha-hydroxylation of sphingolipid-associated very long chain fatty acids. J Biol Chem 272:28281–28288. https://doi.org/10.1074/jbc.272.45.28281

    Article  CAS  PubMed  Google Scholar 

  43. Bard M, Bruner DA, Pierson CA, Lees ND, Biermann B, Frye L, Koegel C, Barbuch R (1996) Cloning and characterization of ERG25, the Saccharomyces cerevisiae gene encoding C-4 sterol methyl oxidase. Proc Natl Acad Sci USA 93:186–190. https://doi.org/10.1073/pnas.93.1.186

    Article  CAS  PubMed  Google Scholar 

  44. Steczkiewicz K, Knizewski L, Rychlewski L, Ginalski K (2010) Tos1 is circularly permuted 1,3-beta-glucanase. Cell Cycle 9:201–204. https://doi.org/10.4161/cc.9.1.10510

    Article  CAS  PubMed  Google Scholar 

  45. Paiva S, Devaux F, Barbosa S, Jacq C, Casal M (2004) Ady2p is essential for the acetate permease activity in the yeast Saccharomyces cerevisiae. Yeast 21:201–210. https://doi.org/10.1002/yea.1056

    Article  CAS  PubMed  Google Scholar 

  46. Oguri S, Minowa MT, Ihara Y, Taniguchi N, Ikenaga H, Takeuchi M (1997) Purification and characterization of UDP-N-acetylglucosamine: alpha1,3-d-mannoside beta1,4-N-acetylglucosaminyltransferase (N-acetylglucosaminyltransferase-IV) from bovine small intestine. J Biol Chem 272:22721–22727. https://doi.org/10.1074/jbc.272.36.22721

    Article  CAS  PubMed  Google Scholar 

  47. Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328:307–317. https://doi.org/10.1016/S0022-2836(03)00307-3

    Article  CAS  PubMed  Google Scholar 

  48. Inuzuka M, Hayakawa M, Ingi T (2005) Serinc, an activity-regulated protein family, incorporates serine into membrane lipid synthesis. J Biol Chem 280:35776–35783. https://doi.org/10.1074/jbc.M505712200

    Article  CAS  PubMed  Google Scholar 

  49. Bossolasco M, Veillette F, Bertrand R, Mesmasson AM (2006) Human TDE1, a TDE1/TMS family member, inhibits apoptosis in vitro and stimulates in vivo tumorigenesis. Oncogene 25:4549–4558. https://doi.org/10.1038/sj.onc.1209488

    Article  CAS  PubMed  Google Scholar 

  50. Nagata M, Kaito C, Sekimizu K (2008) Phosphodiesterase activity of CvfA is required for virulence in Staphylococcus aureus. J Biol Chem 283:2176–2184. https://doi.org/10.1074/jbc.M705309200

    Article  CAS  PubMed  Google Scholar 

  51. Aravind L, Koonin EV (1998) The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem Sci 23:469–472. https://doi.org/10.1016/S0968-0004(98)01293-6

    Article  CAS  PubMed  Google Scholar 

  52. Kuroda M, Hashida-Okado T, Yasumoto R, Gomi K, Kato I, Takesako K (1999) An aureobasidin a resistance gene isolated from Aspergillus, is a homolog of yeast AUR1, a gene responsible for inositol phosphorylceramide (IPC) synthase activity. Mol Gen Genet 261:290–296

    Article  CAS  Google Scholar 

  53. Heidler SA, Radding JA (1995) The AUR1 gene in Saccharomyces cerevisiae encodes dominant resistance to the antifungal agent aureobasidinA (LY295337). Antimicrob Agents Chemother 39:2765–2769. https://doi.org/10.1128/AAC.39.12.2765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Li YH, Han WJ, Gui XW, Wei T, Tang SY, Jin JM (2016) Putative nonribosomal peptide synthetase and cytochrome P450 genes responsible for tentoxin biosynthesis in Alternaria alternata ZJ33. Toxins 8:234. https://doi.org/10.3390/toxins8080234

    Article  CAS  PubMed Central  Google Scholar 

  55. Kulkarni RD, Kelkar HS, Dean RA (2003) An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem Sci 28:118. https://doi.org/10.3390/toxins8080234

    Article  CAS  PubMed  Google Scholar 

  56. Nasser L, Weissman Z, Pinsky M, Amartely H, Dvir H, Kornitzer D (2016) Structural basis of haem-iron acquisition by fungal pathogens. Nat Microbiol 1:16156. https://doi.org/10.1038/NMICROBIOL.2016.156

    Article  CAS  PubMed  Google Scholar 

  57. Kuang WW, Thompson DA, Hoch RV, Weigel RJ (1998) Differential screening and suppression subtractive hybridization identified genes differentially expressed in an estrogen receptor-positive breast carcinoma cell line. Nucleic Acids Res 26:1116–1123. https://doi.org/10.1093/nar/26.4.1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Freemont PS (1993) The RING finger. A novel protein sequence motif related to the zinc finger. Ann NY Acad Sci 684:174–192. https://doi.org/10.1111/j.1749-6632.1993.tb32280.x

    Article  CAS  PubMed  Google Scholar 

  59. Joazeiro CAP, Wing SS, Huang H, Leverson JD, Hunter T, Liu YC (1999) The tyrosine kinase negative regulator c-Cbl as a ring-type, E2-dependent ubiquitin–protein ligase. Science 286:309–312. https://doi.org/10.1126/science.286.5438.309

    Article  CAS  PubMed  Google Scholar 

  60. Shen Q, Uknes SJ, Ho TH (1993) Hormone response complex in a novel abscisic acid and cycloheximide–inducible barley gene. J Biol Chem 268:23652–23660

    CAS  PubMed  Google Scholar 

  61. Gillespie JR, Yokoyama K, Lu K, Eastman RT, Bollinger JG, Van Voorhis WC, Gelb MH, Buckner FS (2007) C-terminal proteolysis of prenylated proteins in trypanosomatids and RNA interference of enzymes required for the post-translational processing pathway of farnesylated proteins. Mol Biochem Parasitol 153:115–124. https://doi.org/10.1016/j.molbiopara.2007.02.009

    Article  CAS  PubMed  Google Scholar 

  62. Pryor EE, Horanyi PS, Clark KM, Fedoriw N, Connelly SM, Koszelak-Rosenblum M, Zhu GY, Malkowski MG, Wiener MC, Dumont ME (2013) Structure of the integral membrane protein CAAX protease Ste24p. Science 339:1600–1604. https://doi.org/10.1126/science.1232048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lee LY, Schaffer PA (1998) A virus with a mutation in the ICP4-binding site in the L/ST, promoter of herpes simplex virus type 1, but not a virus with a mutation in open reading frame P, exhibits cell-type-specific expression of γ134.5 transcripts and latency-associated transcripts. J Virol 72:4250–4264

    Article  CAS  Google Scholar 

  64. Das AK, Helps NR, Cohen PT, Barford D (1996) Crystal structure of the protein serine/threonine phosphatase 2C at 2.0A resolution. EMBO J 15:6798–6809

    Article  CAS  Google Scholar 

  65. Da-Silva AM, Zapella PD, Andrioli LP, Campanha RB, Fiorini LC, Etchebehere LC, da-Costa-Maia JC, Terenzi HF (1999) Searching for the role of protein phosphatases in eukaryotic microorganisms. Braz J Med Biol Res 32:835–839. https://doi.org/10.1590/S0100-879X1999000700006

    Article  CAS  PubMed  Google Scholar 

  66. West JR, Crivellone MD, Ma J, Thomas S (1996) Sequence of the Saccharomyces cerevisiae YTP1 gene encoding a deduced novel type-III integral membrane protein with domains of sequence similarity to mitochondrial electron-transport enzymes. Gene 169:119–124. https://doi.org/10.1016/0378-1119(95)00774-1

    Article  CAS  PubMed  Google Scholar 

  67. Denu JM, Dixon JE (1998) Protein tyrosine phosphatases: mechanisms of catalysis and regulation. Curr Opin Chem Biol 2:633–641. https://doi.org/10.1016/S1367-5931(98)80095-1

    Article  CAS  PubMed  Google Scholar 

  68. Protchenko O, Rodriguezsuarez R, Androphy R, Bussey H, Philpott CC (2006) A screen for genes of heme uptake identifies the FLC family required for import of FAD into the endoplasmic reticulum. J Biol Chem 281:21445–21457. https://doi.org/10.1074/jbc.M512812200

    Article  CAS  PubMed  Google Scholar 

  69. Palmer CP, Aydar E, Djamgoz MB (2005) A microbial TRP-like polycystic-kidney-disease-related ion channel gene. Biochem J 387:211–219. https://doi.org/10.1042/BJ20041710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Hollinger S, Hepler JR (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54:527–559. https://doi.org/10.1124/pr.54.3.527

    Article  CAS  PubMed  Google Scholar 

  71. Gu S, Cifelli C, Wang S, Heximer SP (2009) Rgs proteins: identifying new gaps in the understanding of blood pressure regulation and cardiovascular function. Clin Sci 116:391–399. https://doi.org/10.1042/CS20080272

    Article  CAS  PubMed  Google Scholar 

  72. Sanchez-Pulido L, Martin-Belmonte F, Valencia A, Alonso MA (2002) MARVEL: a conserved domain involved in membrane apposition events. Trends Biochem Sci 27:599–601. https://doi.org/10.1016/S0968-0004(02)02229-6

    Article  CAS  PubMed  Google Scholar 

  73. Heiman MG, Walter P (2000) Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating. J Cell Biol 151:719–730. https://doi.org/10.1083/jcb.151.3.719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Ruffolo CG, Adler B (1996) Cloning, sequencing, expression, and protective capacity of the oma87 gene encoding the Pasteurella multocida 87-kilodalton outer membrane antigen. Infect Immun 64:3161–3167. https://doi.org/10.1016/0162-3109(96)00109-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Flack FS, Loosmore S, Chong P, Thomas WR (1995) The sequencing of the 80-kDa D15 protective surface antigen of haemophilus influenzae. Gene 156:97–99. https://doi.org/10.1016/0378-1119(95)00049-C

    Article  CAS  PubMed  Google Scholar 

  76. Kitamura A, Someya K, Okumura R, Hata M, Takeshita H, Nakajima R (2010) In vitro antifungal activities of D11-2040, a β-1,6-glucan inhibitor, with or without currently available antifungal drugs. Biol Pharm Bull 33:192–197. https://doi.org/10.1248/bpb.33.192

    Article  CAS  PubMed  Google Scholar 

  77. Chen LH, Tsai HC, Yu PL, Chung KR (2017) A major facilitator superfamily transporter-mediated resistance to oxidative stress and fungicides requires Yap1, Skn7, and MAP kinases in the citrus fungal pathogen Alternaria alternata. PLoS ONE 12:e0169103. https://doi.org/10.1371/journal.pone.0169103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Wang MS, Sun XP, Yu DL, Xu JP, Chung KR, Li HY (2016) Genomic and transcriptomic analyses of the tangerine pathotype of Alternaria alternata in response to oxidative stress. Sci Rep 6:32437. https://doi.org/10.1038/srep32437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Wang NY, Lin CH, Chung KR (2010) A G alpha subunit gene is essential for conidiation and potassium efflux but dispensable for pathogenicity of Alternaria alternata on citrus. Curr Genet 56:43–51. https://doi.org/10.1007/s00294-009-0278-2

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from Key Research and Development Program of Hebei Province (19226509D), Project of Beijing Municipal Commission of Education (KZ201911417049), Premium Funding Project for Academic Human Resources Development in Beijing Union University (BPHR2018BZ01), and National Natural Science Foundation of China (21476011).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pingfang Tian.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, R., Zhao, P., Ge, X. et al. Overview of Alternaria alternata Membrane Proteins. Indian J Microbiol 60, 269–282 (2020). https://doi.org/10.1007/s12088-020-00873-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-020-00873-8

Keywords

Navigation