Skip to main content
Log in

BcMctA, a putative monocarboxylate transporter, is required for pathogenicity in Botrytis cinerea

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Monocarboxylate transporters have a central role in mammalian metabolism, but rarely reported in phytopathogenic fungi. In this study, a putative monocarboxylate transporter gene in Botrytis cinerea [B. cinerea MctA (BcMctA)] was identified in the research of a B. cinerea transfer DNA (T-DNA) insertional mutant (74). Disruption of the gene decreased the growth rate on the medium with monocarboxylate (acetate or pyruvate) as the sole carbon sources, but not affected on lactate. The pyruvate contents in BcmctA deletion mutants decreased about 35 % compared with the wild strain. Besides, the conidial yield was increased about two times in BcmctA disruption mutant. The pathogenicity assay indicated that disruption of BcmctA significantly reduced the virulence of B. cinerea on cucumber and tomato leaves. Our results demonstrated that BcMctA is related to pyruvate uptake and pathogenicity of B. cinerea on cucumber and tomato leaves.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aguayo C, Riquelme J, Valenzuela PDT, Hahn M, Moreno ES (2011) Bchex virulence gene of Botrytis cinerea: characterization and functional analysis. J Gen Plant Pathol 77(4):230–238

    Article  Google Scholar 

  • Benito EP, ten Have A, van’t Klooster JW, Van Kan JAL (1998) Fungal and plant gene expression during synchronized infection of tomato leaves by Botrytis cinerea. Eur J Plant Pathol 104(2):207–220

    Article  CAS  Google Scholar 

  • Cássio F, Côrte-Real M, Leão C (1993) Quantitative analysis of proton movements associated with the uptake of weak carboxylic acids: the yeast Candida utilis as a model. Biochim Biophys Acta 1153(1):59–66

    Article  PubMed  Google Scholar 

  • Cui Z, Ding Z, Yang X, Wang K, Zhu T (2009) Gene disruption and characterization of a class V chitin synthase in Botrytis cinerea. Can J Microbiol 55(11):1267–1274

    Article  CAS  PubMed  Google Scholar 

  • Cui Z, Wang Y, Lei N, Wang K, Zhu T (2013) Botrytis cinerea chitin synthase BcChsVI is required for normal growth and pathogenicity. Curr Genet 59(3):119–128

    Article  CAS  PubMed  Google Scholar 

  • Davis DA (2009) How human pathogenic fungi sense and adapt to pH: the link to virulence. Curr Opin Microbiol 12(4):365–370

    Article  CAS  PubMed  Google Scholar 

  • Friesema EC, Ganguly S, Abdalla A, Manning Fox JE, Halestrap AP, Visser TJ (2003) Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J Biol Chem 278(41):40128–40135

    Article  CAS  PubMed  Google Scholar 

  • Giesbert S, Schumacher J, Kupas V, Espino J, Segmüller N, Haeuser-Hahn I, Schreier PH, Tudzynski P (2012) Identification of pathogenesis-associated genes by T-DNA-mediated insertional mutagenesis in Botrytis cinerea: a type 2A phosphoprotein phosphatase and an SPT3 transcription factor have significant impact on virulence. Mol Plant Microbe Interact 25(4):481–495

    Article  CAS  PubMed  Google Scholar 

  • Halestrap AP (2012) The monocarboxylate transporter family—Structure and functional characterization. IUBMB Life 64(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Halestrap AP (2013) The SLC16 gene family—Structure, role and regulation in health and disease. Mol Aspects Med 34(2–3):337–349

    Article  CAS  PubMed  Google Scholar 

  • Halestrap AP, Meredith D (2004) The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 447(5):619–628

    Article  CAS  PubMed  Google Scholar 

  • Halestrap AP, Price NT (1999) The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem J 343(Pt 2):281–299

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harren K, Schumacher J, Tudzynski B (2012) The Ca2+/calcineurin-dependent signaling pathway in the gray mold Botrytis cinerea: the role of calcipressin in modulating calcineurin activity. PLoS One 7(7):e41761

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jackson MA, Schisler DA (1992) The composition and attributes of Colletotrichum truncatum spores are altered by the nutritional environment. Appl Environ Microbiol 58(7):2260–2265

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jin K, Zhang Y, Fang W, Luo Z, Zhou Y, Pei Y (2010) Carboxylate transporter gene JEN1 from the entomopathogenic fungus Beauveria bassiana is involved in conidiation and virulence. Appl Environ Microbiol 76(1):254–263

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim DK, Kanai Y, Chairoungdua A, Matsuo H, Cha SH, Endou H (2001) Expression cloning of a Na+-independent aromatic amino acid transporter with structural similarity to H+/monocarboxylate transporters. J Biol Chem 276(20):17221–17228

    Article  CAS  PubMed  Google Scholar 

  • Kim YT, Prusky D, Rollins JA (2007) An activating mutation of the Sclerotinia sclerotiorum pac1 gene increases oxalic acid production at low pH but decreases virulence. Mol Plant Pathol 8(5):611–622

    Article  CAS  PubMed  Google Scholar 

  • Landraud P, Chuzeville S, Billon-Grande G, Poussereau N, Bruel C (2013) Adaptation to pH and role of PacC in the rice blast fungus Magnaporthe oryzae. PLoS ONE 8(7):e69236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu YG, Whittier RF (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments form P1 and YAC clones for chromosome walking. Genomics 25(3):674–681

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Leroux P, Fillinger S (2008) The HOG1-like MAP kinase Sak1 of Botrytis cinerea is negatively regulated by the upstream histidine kinase Bos1 and is not involved in dicarboximide and phenylpyrrole resistance. Fungal Genet Biol 45(7):1062–1074

    Article  CAS  PubMed  Google Scholar 

  • Makuc J, Paiva S, Schauen M, Kramer R, Andre B, Casal M, Leao C, Boles E (2001) The putative monocarboxylate permeases of the yeast Saccharomyces cerevisiae do not transport monocarboxylic acids across the plasma membrane. Yeast 18(12):1131–1143

    Article  CAS  PubMed  Google Scholar 

  • Manteau S, Abouna S, Lambert B, Legendre L (2003) Differential regulation by ambient pH of putative virulence factor secretion by the phytopathogenic fungus Botrytis cinerea. FEMS Microbiol Ecol 43(3):359–366

    Article  CAS  PubMed  Google Scholar 

  • Meredith D, Christian HC (2008) The SLC16 monocaboxylate transporter family. Xenobiotica 38(7–8):1072–1106

    Article  CAS  PubMed  Google Scholar 

  • Michielse CB, Becker M, Heller J, Moraga J, Collado IG, Tudzynski P (2011) The Botrytis cinerea Reg1 protein, a putative transcriptional regulator, is required for pathogenicity, conidiogenesis, and the production of secondary metabolites. Mol Plant Microbe Interact 24(9):1074–1085

    Article  CAS  PubMed  Google Scholar 

  • Mouchiroud L, Molin L, Kasturi P, Triba MN, Dumas ME, Wilson MC, Halestrap AP, Roussel D, Masse I, Dalliere N, Segalat L, Billaud M, Solari F (2010) Pyruvate imbalance mediates metabolic reprogramming and mimics lifespan extension by dietary restriction in Caenorhabditis elegans. Aging Cell 10(1):39–54

    Article  PubMed  Google Scholar 

  • Price NT, Jackson VN, Halestrap AP (1998) Cloning and sequencing of four new mammalian monocarboxylate transporter (MCT) homologues confirms the existence of a transporter family with an ancient past. Biochem J 329(Pt 2):321–328

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reihl P, Stolz J (2005) The monocarboxylate transporter homolog Mch5p catalyzes riboflavin (vitamin B2) uptake in Saccharomyces cerevisiae. J Biol Chem 280(48):39809–39817

    Article  CAS  PubMed  Google Scholar 

  • Safavi SA, Shah FA, Pakdel AK, Rasoulian GR, Bandani AR, Butt TM (2007) Effect of nutrition on growth and virulence of the entomopathogenic fungus Beauveria bassiana. FEMS Microbiol Lett 270(1):116–123

    Article  CAS  PubMed  Google Scholar 

  • Semighini CP, Goldman MH, Goldman GH (2004) Multi-copy suppression of an Aspergillus nidulans mutant sensitive to camptothecin by a putative monocarboxylate transporter. Curr Microbiol 49(4):229–233

    Article  CAS  PubMed  Google Scholar 

  • Shah FA, Wang CS, Butt TM (2005) Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol Lett 251(2):259–266

    Article  CAS  PubMed  Google Scholar 

  • Verhoeff K, Leeman M, van Peer R, Posthuma L, Schot N, van Eijk GW (1988) Changes in pH and the production of organic acids during colonization of tomato petioles by Botrytis cinerea. J Phytopathol 122:327–336

    Article  CAS  Google Scholar 

  • Visser WE, Friesema EC, Jansen J, Visser TJ (2007) Thyroid hormone transport by monocarboxylate transporters. Best Pract Res Clin Endocrinol Metab 21(2):223–236

    Article  CAS  PubMed  Google Scholar 

  • Williamson B, Tudzynski B, Tudzynski P, van Kan JA (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8(5):561–580

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Chen Y, Ma Z (2013) Involvement of BcVeA and BcVelB in regulating conidiation, pigmentation and virulence in Botrytis cinerea. Fungal Genet Biol 50:63–71

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant from the Scientific Research Foundation of Zhejiang Province (No. LY12C14008) and National Nature Science Foundation of China (No. 31272002).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zhifeng Cui or Tingheng Zhu.

Additional information

Communicated by M. Kupiec.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cui, Z., Gao, N., Wang, Q. et al. BcMctA, a putative monocarboxylate transporter, is required for pathogenicity in Botrytis cinerea . Curr Genet 61, 545–553 (2015). https://doi.org/10.1007/s00294-015-0474-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-015-0474-1

Keywords

Navigation