Russian Journal of Genetics

, Volume 54, Issue 6, pp 618–628 | Cite as

Cold Temperature Regulation of Zoospore Release in Phytophthora sojae: The Genes That Differentially Expressed by Cold Temperature

  • Ya. Wang
  • X. Jin
  • H. Rui
  • T. LiuEmail author
  • J. Hou
Genetic of Microorganisms


Cold temperature is an important environmental factor that affects the lives of many organisms in various ways. In this study, cold temperature was found to promote the release of zoospores from Phytophthora sojae sporangia. To better understand this phenomenon, Illumina sequencing was used to examine the differential expression of P. sojae genes between three control libraries and three cold temperature (4°C) treatment libraries. The six libraries generated 1.04, 1.17, 1.11, 0.96, 1.23, and 1.13 million clean sequencing reads. Comparison of the gene expression levels between the control and cold treatment conditions revealed 175 differentially expressed genes (DEGs), including 38 up-regulated and 137 down-regulated genes in the cold temperature group compared to the control group. The DEGs were functionally classified using the Clusters of Orthologous Groups (COG) database, and the results indicated that these DEGs were mainly involved in signal transduction, translation, ribosomal structure and biogenesis, transcription and carbohydrate transport and metabolism. KEGG pathway analysis showed that the top 20 pathways significantly enriched in DEGs included amino sugar and nucleotide sugar metabolism, arginine and proline metabolism, and starch and sucrose metabolism. Some of the DEGs are involved in the release of zoospores from P. sojae sporangia is discussed in the present work. This information will be helpful for understanding the mechanism of zoospore release induced by cold temperature.


cold temperature Phytophthora sojae zoospore release differential gene expression 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Kaufmann, M.J. and Gerdemann, J.W., Root and stem rot of soybean caused by Phytophthora sojae sp., Phytopathology, 1958, vol. 48, no. 4, pp. 201–208.Google Scholar
  2. 2.
    Schmitthenner, A.F., Problems and progress in control of Phytophthora root rot of soybean, Plant Dis., 1985, vol. 69, no. 4, pp. 362–368.Google Scholar
  3. 3.
    Jee, H., Occurrence of Phytophthora root on soybean (Glycine max) and identification of the causal fungus, J. Crop Protect., 1998, vol. 40, no. 1, pp. 16–22.Google Scholar
  4. 4.
    Huang, J., Guo, N., Li, Y.H., et al., Phenotypic evaluation and genetic dissection of resistance to Phytophthora sojae in the Chinese soybean mini core collection, BMC Genet., 2016, vol. 17, no. 1, pp. 1–14.Google Scholar
  5. 5.
    Shen, C.Y. and Su, Y.C., Discovery and preliminary studies of Phytophthora megasperma on soybean in China, Acta Phytopathol. Sin.,1991, vol. 4, p. 298.Google Scholar
  6. 6.
    Wen, J.Z. and Zhang, M.H., The pathogen causing Phytophthora disease of soybean, Chin. J. Oil Crop Sci., 1998, vol. 4, pp. 40–45.Google Scholar
  7. 7.
    Xu, X.H., Qu, J.J., and Zhang, X.P., Progress of research on Phytophthora root rot, J. Northeast Agric. Univ., 2003, vol. 34, no. 4, pp. 474–477.Google Scholar
  8. 8.
    Dai, Y., Liu, T.F., Zhang, L.F., et al., First report of Phytophthora root and stem caused by Phytophthora sojae on soybean in Taihe, China, Plant Dis., 2015, vol. 99, no. 12, p. 1861.Google Scholar
  9. 9.
    Morris, P.F. and Ward, E.W.B., Chemoattraction of zoospores of the soybean pathogen, Phytophthora sojae, by isoflavones, Physiol. Mol. Plant Pathol., 1992, vol. 40, no. 1, pp. 17–22.Google Scholar
  10. 10.
    Judelson, H.S. and Tani, S., Transgene-induced silencing of the zoosporogenesis-specific NIFC gene cluster of Phytophthora infestans involves chromatin alterations, Eukaryot Cell, 2007, vol. 6, no. 7, pp. 1200–1209.Google Scholar
  11. 11.
    Dorrance, A.E., Mills, D., Robertson, A.E., et al., Phytophthora root and stem rot of soybean, Plant Health Instr., 2007, pp. 1–10.Google Scholar
  12. 12.
    Hardham, A.R., Cell biology of plant–oomycete interactions, Cell Microbiol., 2007, vol. 9, no. 1, pp. 31–39.Google Scholar
  13. 13.
    Tyler, B.M., Phytophthora sojae: root rot pathogen of soybean and model oomycete, Mol. Plant Pathol., 2007, vol. 8, no. 1, pp.1–8.Google Scholar
  14. 14.
    Zhang, M., Lu, J., and Tao, K., A Myb transcription factor of Phytophthora sojae, regulated by MAP kinase PsSAK1, is required for zoospores development, PLoS One, 2012, vol. 7, no. 6, p. 40246.Google Scholar
  15. 15.
    Ribeiro, O.K., Physiology of asexual sporulation and spore germination in Phytophthora, Plant Pathog. Fungi, 1983, pp. 55–70.Google Scholar
  16. 16.
    Tani, S. and Judelson, H., Activation of zoosporogenesis-specific genes in Phytophthora infestans involves a 7-nucleotide promoter motif and cold-induced membrane rigidity, Eukaryot Cell, 2006, vol. 5, no. 4, pp. 745–752.Google Scholar
  17. 17.
    Lan, C.Z., Chen, Q.H., Zhao, J., et al., Studies on the methods for stimulating large a mounts of sporangia of Phytophthora sojae, Acta Agric. Univ. Jiangxiensis, 2007, vol. 29, no. 4, pp. 557–560.Google Scholar
  18. 18.
    Zuo, Y.H., Jian, Z.J., and Liu, X.R., Studies on production condition of zoospores of Phytophthora sojae, Acta Phytopathol. Sin., 2001, vol. 31, no. 3, pp. 241–245.Google Scholar
  19. 19.
    Belova, I.V., Tochilina, A.G., Solovyeva, I.V., et al., Lactobacillus fermentum 90 TC-4 taxonomic status confirmation using whole genome sequencing and MALDI TOF mas spectrum, Russ. J. Genet., 2016, vol. 52, no. 9, pp. 907–913.Google Scholar
  20. 20.
    Omelchenko, D.O., Rzhaninova, A.A., Goldshtein, D.V., et al., Comparative transcriptome pairwise analysis of spontaneously transformed multipotent stromal cells from human adipose tissue, Russ. J. Genet., 2014, vol. 50, no. 1, pp. 96–104.Google Scholar
  21. 21.
    Yu, Y., Huang, W.G., Chen, H.Y., et al., Identification of differentially expressed genes in flax (Linum usitatissimum L.) under saline-alkaline stress by digital gene expression, Gene, 2014, vol. 549, no. 1, pp. 113–122.Google Scholar
  22. 22.
    Qin, Y.F., Fang, H.M., Tian, Q.N., et al., Transcriptome profiling and digital gene expression by deepsequencing in normal/regenerative tissues of planarian Dugesia japonica, Genomics, 2011, vol. 97, no. 6, pp. 364–371.Google Scholar
  23. 23.
    Yan, H., Zhang, H., Chen, M., et al., Transcriptome and gene expression analysis during flower blooming in Rosa chinensis ‘Pallida,’ Gene, 2014, vol. 504, no. 1, pp. 96–103.Google Scholar
  24. 24.
    Kim, D., Pertea, G., Trapnell, C., et al., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions, Genome Biol., 2013, vol. 14, no. 4, pp. 295–311.Google Scholar
  25. 25.
    Judelson, H.S. and Blanco, F.A., The spores of Phytophthora: weapons of the plant destroyer, Nat. Rev. Microbio, 2005, vol. 3, no. 1, pp. 47–58.Google Scholar
  26. 26.
    Tani, S., Yatzkan, E., and Judelson, H.S., Multiple pathways regulate the induction of genes during zoosporogenesis in Phytophthora infestans, Mol. Plant–Microbe Interact., 2004, vol. 17, no. 3, pp. 330–337.Google Scholar
  27. 27.
    Judelson, H.S. and Roberts, S., Novel protein kinase induced during sporangial cleavage in the oomycete Phytophthora infestans, Eukaryot. Cell, 2002, vol. 1, no. 5, pp. 687–695.Google Scholar
  28. 28.
    Chinnusamy, V., Zhu, J.H., and Zhu, J.K., Cold stress regulation of gene expression in plants, Trends Plant Sci., 2007, vol. 12, no. 10, pp. 444–451.Google Scholar
  29. 29.
    Wang, J.M., Yang, Y., Liu, X.H., et al., Transcriptome profiling of the cold response and signaling pathways in Lilium lancifolium, BMC Genomics, 2014, vol. 15, no. 1, pp. 1–20.Google Scholar
  30. 30.
    Suzuki, N. and Mittler, R., Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction, Physiol. Plant., 2006, vol. 126, no. 1, pp. 45–51.Google Scholar
  31. 31.
    Barrett, K.E., Barman, S.M., Boitano, S., et al., Overview of cellular physiology in medical physiology, in Ganong’s Review of Medical Physiology, Barrett, K.E., Barman, S.M., Boitano, S., and Brooks, H., Eds., 2011.Google Scholar
  32. 32.
    Campos, P.S., Quartin, V., Ramalho, J.C., et al., Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants, J. Plant Physiol., 2003, vol. 160, no. 3, pp. 283–292.Google Scholar
  33. 33.
    Liu, Y.B., Liu, M.L., Li, X.R., et al., Identification of differentially expressed genes in leaf of Reaumuria soongorica under PEG-induced drought stress by digital gene expression profilin, PLoS One, 2013, vol. 9, no. 4. e94277Google Scholar
  34. 34.
    Fulda, S., Gorman, A.M., Hori, O., et al., Cellular stress responses: cell survival and cell death, Int. J. Cell Biol., 2010.Google Scholar
  35. 35.
    Kolesnikov, Y.S., Nokhrina, K.P., Kretynin, S.V., et al., Molecular structure of phospholipase D and regulatory mechanisms of its activity in plant and animal cells, Biochemistry, 2012, vol. 77, no. 1, pp. 1–14.Google Scholar
  36. 36.
    Lee, S., Hirt, H., and Lee, Y., Phosphatidic acid activates a wound-activated MAPK in Glycine max, Plant J. Cell Mol. Biol., 2001, vol. 26, no. 5, pp. 479–486.Google Scholar
  37. 37.
    Sang, Y., Cui, D., and Wang, X., Phospholipase D and phosphatidicacid-mediated generation of superoxide in Arabidopsis, Plant Physiol., 2001, vol. 126, no. 4, pp. 1449–1458.Google Scholar
  38. 38.
    Yamaguchi, T., Minami, E., Shibuya, N., Activation of phospholipases by N-acetylchitooligosaccharide elicitor in suspension-cultured rice cells mediates reactive oxygen generation, Physiol. Plant., 2003, vol. 118, no. 3, pp. 361–370.Google Scholar
  39. 39.
    Bocckino, S., Blackmore, P., Wilson, P., et al., Phosphatidate accumulation in hormone-treated hepatocytes via a phospholipase D mechanism, J. Biol. Chem., 1987, vol. 118, no. 3, pp. 15309–15315Google Scholar
  40. 40.
    Hodgkin, M., Pettitt, T., Martin, A., et al., Diacylglycerols and phosphatidates: which molecular species are intracellular messengers?, Trends Biochem. Sci., 1998, vol. 23, no. 6, pp. 200–204.Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  1. 1.Heilongjiang Bayi Agricultural UniversityDaqing, HeilongjiangP.R. China
  2. 2.Heilongjiang Academy of Agricultural SciencesDaqing, HeilongjiangP.R. China
  3. 3.Hainan UniversityHaikou, Hainan ProvinceP.R. China

Personalised recommendations