Identification and Expression Analysis of Heavy Metal-associated Isoprenylated Plant Proteins(HIPPs) Genes in Populus

doi:10.7525/j.issn.1673-5102.2019.06.017

Abstract

Abstract: Metal chaperones play key roles in plant physiological activities, and could bind metal ions and transport them to target proteins in order to maintain the metal ions homeostasis of cells. Currently, the properties and function analysis of the metal chaperones HIPP (heavy metal-associated isoprenylated plant protein) is mostly limited to the model plant Arabidopsis thaliana. In this study, 14 PtHIPPs were identified in Populus trichocarpa, all of which had two conserved metal ion binding motif MXCXXC, as well as the conserved isoprenylation motif in the carboxyl terminal. The amino terminal of PtHIPPs was form the βαββαβ secondary structure. Some PtHIPPs had lysine-rich and/or glycine-rich regions. PtHIPPs proteins could be divided into three subgroups according to gene structure, protein conservation motifs and phylogenetic analysis. The tissue-specific expression data of PlantGenIE and the results of fluorescence quantitative PCR identification showed that PtHIPPs genes of P.trichocarpa and PnHIPPs genes of Populus simonii×Populus nigra had tissue-specific expression characterizations and differences. In addition, the expression patterns of PnHIPPs in different tissues of P.simonii×P.nigra seedlings were changed after treated with copper deficiency or copper excess conditions for different times. This study provided theoretical groundwork for identifying the roles of HIPPs proteins in maintaining copper homeostasis in woody model plant Populus.

Key words: Populus, HIPPs, bioinformatics analysis, copper stress, gene expression

CLC Number:

S792.11

WANG Qi, XU Zhi-Ru, CHEN Jin-Yuan, ZHANG Shuang, HUANG Jia-Huan, LIU Guan-Jun. Identification and Expression Analysis of Heavy Metal-associated Isoprenylated Plant Proteins(HIPPs) Genes in Populus[J]. Bulletin of Botanical Research, 2019, 39(6): 935-946.

References

1. Huffman D L,O'halloran T V. Function,structure,and mechanism of intracellular copper trafficking proteins[J]. Annual Review of Biochemistry,2001,70:677-701.
2. Dupont C L,Butcher A,Valas R E,et al. History of biological metal utilization inferred through phylogenomic analysis of protein structures[J]. Proceedings of the National Academy of Sciences of the United States of America,2010,107(23):10567-10572.
3. Barth O,Vogt S,Uhlemann R,et al. Stress induced and nuclear localized HIPP26 from Arabidopsis thaliana interacts via its heavy metal associated domain with the drought stress related zinc finger transcription factor ATHB29[J]. Plant Molecular Biology,2009,69(1-2):213-226.
4. Tehseen M,Cairns N,Sherson S,et al. Metallochaperone-like genes in Arabidopsis thaliana[J]. Metallomics,2010,2(8):556-564.
5. De Abreu-Neto J B,Turchetto-Zolet A C,De Oliveira L F V,et al. Heavy metal-associated isoprenylated plant protein(HIPP):characterization of a family of proteins exclusive to plants[J]. FEBS Journal,2013,280(7):1604-1616.
6. Gao W,Xiao S,Li H Y,et al. Arabidopsis thaliana acyl-CoA-binding protein ACBP2 interacts with heavy-metal-binding farnesylated protein AtFP6[J]. New Phytologist,2009,181(1):89-102.
7. Crowell D N. Functional implications of protein isoprenylation in plants[J]. Progress in Lipid Research,2000,39(5):393-408.
8. Suzuki N,Yamaguchi Y,Koizumi N,et al. Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis[J]. The Plant Journal,2002,32(2):165-173.
9. Dykema P E,Sipes P R,Marie A,et al. A new class of proteins capable of binding transition metals[J]. Plant Molecular Biology,1999,41(1):139-150.
10. Zhang X,Feng H,Feng C,et al. Isolation and characterisation of cDNA encoding a wheat heavy metal-associated isoprenylated protein involved in stress responses[J]. Plant Biology,2015,17(6):1176-1186.
11. Radakovic Z S,Anjam M S,Escobar E,et al. Arabidopsis HIPP27 is a host susceptibility gene for the beet cyst nematode Heterodera schachtii[J]. Molecular Plant Pathology,2018,19(8):1917-1928.
12. Cowan G H,Roberts A G,Jones S,et al. Potato mop-top virus co-opts the stress sensor HIPP26 for long-distance movement[J]. Plant Physiology,2018,176(3):2052-2070.
13. Barth O,Zschiesche W,Siersleben S,et al. Isolation of a novel barley cDNA encoding a nuclear protein involved in stress response and leaf senescence[J]. Physiologia Plantarum,2004,121(2):282-293.
14. Zschiesche W,Barth O,Daniel K,et al. The zinc-binding nuclear protein HIPP3 acts as an upstream regulator of the salicylate-dependent plant immunity pathway and of flowering time in Arabidopsis thaliana[J]. New Phytologist,2015,207(4):1084-1096.
15. Puig S,Mira H,Dorcey E,et al. Higher plants possess two different types of ATX1-like copper chaperones[J]. Biochemical and Biophysical Research Communications,2007,354(2):385-390.
16. Himelblau E,Mira H,Lin S J,et al. Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis[J]. Plant Physiology,1998,117(4):1227-1234.
17. Abdel-Ghany S E,Burkhead J L,Gogolin K A,et al. AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7[J]. FEBS Letters,2005,579(11):2307-2312.
18. Shin L J,Lo J C,Yeh K C. Copper chaperone antioxidant protein1 is essential for copper homeostasis[J]. Plant Physiology,2012,159(3):1099-1110.
19. Taylor G. Populus:Arabidopsis for forestry. Do we need a model tree?[J]. Annals of Botany,2002,90(6):681-689.
20. Tuskan G A,Difazio S,Jansson S,et al. The genome of black cottonwood,Populus trichocarpa(Torr. & Gray)[J]. Science,2006,313(5793):1596-1604.
21. Xu Z R,Gao L Y,Tang M Q,et al. Genome-wide identification and expression profile analysis of CCH gene family in Populus[J]. PeerJ,2017,5(1):e3962.
22. Larson P R,Isebrands J G. The plastochron index as applied to developmental studies of cottonwood[J]. Canadian Journal of Forest Research,1971,1(1):1-11.
23. Goodstein D M,Shu S Q,Howson R,et al. Phytozome:a comparative platform for green plant genomics[J]. Nucleic Acids Research,2012,40(D1):D1178-D1186.
24. Livak K J,Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-ΔΔCT method[J]. Methods,2001,25(4):402-408.
25. 丁一巍,詹亚光,张佳薇,等. 水曲柳2个PLT转录因子基因的克隆及表达分析[J]. 植物研究,2019,39(1):139-147. Ding Y W,Zhan Y G,Zhang J W,et al. Cloning and expression analysis of two PLT transcription factors genes in Fraxinus mandshurica[J]. Bulletin of Botanical Research,2019,39(1):139-147.
26. Sundell D,Mannapperuma C,Netotea S,et al. The plant genome integrative explorer resource:PlantGenIE. org[J]. New Phytologist,2015,208(4):1149-1156.
27. Harrison M D,Jones C E,Solioz M,et al. Intracellular copper routing:the role of copper chaperones[J]. Trends in Biochemical Sciences,2000,25(1):29-32.
28. Chu C C,Lee W C,Guo W Y,et al. A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis[J]. Plant Physiology,2005,139(1):425-436.
29. Lin S J,Culotta V C. The ATX1 gene of Saccharomyces cerevisiae encodes a small metal homeostasis factor that protects cells against reactive oxygen toxicity[J]. Proceedings of the National Academy of Sciences of the United States of America,1995,92(9):3784-3788.
30. Arnesano F,Banci L,Bertini I,et al. Characterization of the binding interface between the copper chaperone Atx1 and the first cytosolic domain of Ccc2 ATPase[J]. The Journal of Biological Chemistry,2001,276(44):41365-41376.
31. Hung I H,Casareno R L B,Labesse G,et al. HAH1 is a copper-binding protein with distinct amino acid residues mediating copper homeostasis and antioxidant defense[J]. The Journal of Biological Chemistry,1998,273(3):1749-1754.
32. 朱雅婧,周亚丽,刘骕骦,等. GmHMADP参与高温高湿下大豆种子活力形成及铜镉胁迫响应的研究[J]. 中国农业科学,2018,51(14):2642-2654. Zhu Y J,Zhou Y L,Liu S S,et al. GmHMADP involved in seed vigor formation of soybean under high temperature and humidity stress and its study responsive to copper and cadmium stress[J]. Scientia Agricultura Sinica,2018,51(14):2642-2654.

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