Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

In silico characterisation and functional validation of chilling tolerant divergence 1 (COLD1) gene in monocots during abiotic stress

P. Anunathini A , V. M. Manoj B , T. S. Sarath Padmanabhan B , S. Dhivya A , J. Ashwin Narayan B , C. Appunu B C and R. Sathishkumar A C
+ Author Affiliations
- Author Affiliations

A Plant Genetic Engineering Laboratory, Department of Biotechnology, Bharathiar University, Coimbatore, India.

B Genetic Transformation Lab, Division of Crop Improvement, ICAR-Sugarcane Breeding Institute, Coimbatore, India.

C Corresponding authors. Emails: rsathish@buc.edu.in; cappunu@gmail.com

Functional Plant Biology 46(6) 524-532 https://doi.org/10.1071/FP18189
Submitted: 16 July 2018  Accepted: 24 January 2019   Published: 4 March 2019

Abstract

The G protein-coupled receptor is one of the major transmembrane proteins in plants. It consists of an α subunit, a β subunit and three γ subunits. Chilling tolerant divergence 1 (COLD1) includes a Golgi pH receptor (GPHR) domain, which maintains cell membrane organisation and dynamics, along with abscisic acid linked G protein-coupled receptor (ABA_GPCR) that regulates the signalling pathways during cold stress. In the present study, we performed characterisation of a homologous COLD1 from the economically important monocot species Oryza sativa L., Zea mays L., Sorghum bicolor (L.) Moench and Erianthus arundinaceus (L.) Beauv. IK 76-81, a wild relative of Saccharum. COLD1 was isolated from E. arundinaceus IK 76-81, analysed for its evolution, domain, membrane topology, followed by prediction of secondary, tertiary structures and functionally validated in all four different monocots. Gene expression studies of COLD1 revealed differential expression under heat, drought, salinity and cold stresses in selected monocots. This is the first study on regulation of native COLD1 during abiotic stress in monocots, which has opened up new leads for trait improvement strategies in this economically important crop species.

Additional keywords: abiotic stress, bioinformatics, proline, qRT-PCR.


References

Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell 15, 63–78.
Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling.Crossref | GoogleScholarGoogle Scholar | 12509522PubMed |

Barkla BJ, Pantoja O (2011) Plasma membrane and abiotic stress. In ‘The plant plasma membrane’. pp. 457–470. (Springer: Heidelberg, Germany)

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar |

Chandra S, Dutta AK, Chandrashekara KN, Acharya K (2017) In silico characterization, homology modeling of Camellia sinensis chitinase and its evolutionary analyses with other plant chitinases. Proceedings of the National Academy of Sciences. India. Section B, Biological Sciences 87, 685–695.
In silico characterization, homology modeling of Camellia sinensis chitinase and its evolutionary analyses with other plant chitinases.Crossref | GoogleScholarGoogle Scholar |

Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Science 2, 1511–1519.
Verification of protein structures: patterns of nonbonded atomic interactions.Crossref | GoogleScholarGoogle Scholar | 8401235PubMed |

Finkelstein R (2013) Abscisic acid synthesis and response. In ‘The Arabidopsis book’. pp. 1–36 (American Society of Plant Biologists: Rockville, MD, USA)

Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In ‘The proteomics protocols handbook’. pp. 571–607. (Humana Press: New York)

Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signaling & Behavior 7, 1456–1466.
Role of proline under changing environments: a review.Crossref | GoogleScholarGoogle Scholar |

Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends in Plant Science 12, 343–351.
Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA.Crossref | GoogleScholarGoogle Scholar | 17629540PubMed |

Hooda V, Babu Gundala P, Chinthala P (2012) Sequence analysis and homology modeling of peroxidase from Medicago sativa. Bioinformation 8, 974–979.
Sequence analysis and homology modeling of peroxidase from Medicago sativa.Crossref | GoogleScholarGoogle Scholar | 23275690PubMed |

Hudson WH, Ortlund EA (2014) The structure, function and evolution of proteins that bind DNA and RNA. Nature Reviews. Molecular Cell Biology 15, 749–760.
The structure, function and evolution of proteins that bind DNA and RNA.Crossref | GoogleScholarGoogle Scholar | 25269475PubMed |

Jiang M, Zhang J (2003) Cross‐talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid‐induced antioxidant defence in leaves of maize seedlings. Plant, Cell & Environment 26, 929–939.
Cross‐talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid‐induced antioxidant defence in leaves of maize seedlings.Crossref | GoogleScholarGoogle Scholar |

Julius D, Nathans J (2011) Signaling by sensory receptors. Cold Spring Harbor Perspectives in Biology 4, 1–14.

Källberg M, Wang H, Wang S, Peng J, Wang Z, Lu H, Xu J (2012) Template-based protein structure modeling using the RaptorX web server. Nature Protocols 7, 1511–1522.
Template-based protein structure modeling using the RaptorX web server.Crossref | GoogleScholarGoogle Scholar | 22814390PubMed |

Kandpal RP, Rao NA (1985) Alterations in the biosynthesis of proteins and nucleic acids in finger millet (Eleucine coracana) seedlings during water stress and the effect of proline on protein biosynthesis. Plant Science 40, 73–79.
Alterations in the biosynthesis of proteins and nucleic acids in finger millet (Eleucine coracana) seedlings during water stress and the effect of proline on protein biosynthesis.Crossref | GoogleScholarGoogle Scholar |

Kruse M, Strandberg M, Strandberg B (2000) Ecological effects of allelopathic plants – a review. NERI Technical Report 315. pp. 1–66. National Environmental Research Institute, Sikeborg, Denmark.

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Levin JM, Robson B, Garnier J (1986) An algorithm for secondary structure determination in proteins based on sequence similarity. FEBS Letters 205, 303–308.
An algorithm for secondary structure determination in proteins based on sequence similarity.Crossref | GoogleScholarGoogle Scholar | 3743779PubMed |

Li Q, Huang J, Liu S, Li J, Yang X, Liu Y, Liu Z (2011) Proteomic analysis of young leaves at three developmental stages in an albino tea cultivar. Proteome Science 9, 44
Proteomic analysis of young leaves at three developmental stages in an albino tea cultivar.Crossref | GoogleScholarGoogle Scholar | 21806834PubMed |

Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxidants & Redox Signalling 19, 998–1011.
Proline mechanisms of stress survival.Crossref | GoogleScholarGoogle Scholar |

Liu X, Yue Y, Li B, Nie Y, Li W, Wu WH, Ma L (2007) AG protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315, 1712–1716.
AG protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid.Crossref | GoogleScholarGoogle Scholar | 17347412PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Lovell SC, Davis IW, Arendall WB, De Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC (2003) Structure validation by Cα geometry: φ, ψ and Cβ deviation. Proteins 50, 437–450.
Structure validation by Cα geometry: φ, ψ and Cβ deviation.Crossref | GoogleScholarGoogle Scholar | 12557186PubMed |

Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J (2015) COLD1 confers chilling tolerance in rice. Cell 160, 1209–1221.
COLD1 confers chilling tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 25728666PubMed |

Maeda Y, Ide T, Koike M, Uchiyama Y, Kinoshita T (2008) GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus. Nature Cell Biology 10, 1135–1145.
GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus.Crossref | GoogleScholarGoogle Scholar | 18794847PubMed |

Matsunami H, Kobayashi M, Tsuruta SI, Terajima Y, Sato H, Ebina M, Ando S (2018) Overwintering ability and high-yield biomass production of Erianthus arundinaceus in a temperate zone in Japan. BioEnergy Research 11, 467–479.
Overwintering ability and high-yield biomass production of Erianthus arundinaceus in a temperate zone in Japan.Crossref | GoogleScholarGoogle Scholar |

McCudden CR, Hains MD, Kimple RJ, Siderovski DP, Willard FS (2005) G-protein signaling: back to the future. Cellular and Molecular Life Sciences 62, 551–577.
G-protein signaling: back to the future.Crossref | GoogleScholarGoogle Scholar | 15747061PubMed |

Netting AG (2000) pH, abscisic acid and the integration of metabolism in plants under stressed and non‐stressed conditions: cellular responses to stress and their implication for plant water relations. Journal of Experimental Botany 51, 147–158.
pH, abscisic acid and the integration of metabolism in plants under stressed and non‐stressed conditions: cellular responses to stress and their implication for plant water relations.Crossref | GoogleScholarGoogle Scholar | 10938821PubMed |

Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. The Plant Cell 7, 173–182.
Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element.Crossref | GoogleScholarGoogle Scholar | 7756828PubMed |

Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136, 136–148.
Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19135895PubMed |

Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8, 785–786.
SignalP 4.0: discriminating signal peptides from transmembrane regions.Crossref | GoogleScholarGoogle Scholar | 21959131PubMed |

Port JA, Parker MS, Kodner RB, Wallace JC, Armbrust EV, Faustman EM (2013) Identification of G protein-coupled receptor signaling pathway proteins in marine diatoms using comparative genomics. BMC Genomics 14, 503
Identification of G protein-coupled receptor signaling pathway proteins in marine diatoms using comparative genomics.Crossref | GoogleScholarGoogle Scholar | 23883327PubMed |

Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A (2012) The Pfam protein families database. Nucleic Acids Research 40, D290–D301.
The Pfam protein families database.Crossref | GoogleScholarGoogle Scholar | 22127870PubMed |

Rajagopal V, Andersen AS (1978) Does abscisic acid influence proline accumulation in stressed leaves? Planta 143, 85–88.
Does abscisic acid influence proline accumulation in stressed leaves?Crossref | GoogleScholarGoogle Scholar | 24408265PubMed |

Rezende ALS, Rodrigues Soares JD, dos Santos HO, Pasqual M, Braga RA, Reis RO, Rodrigues FA, Ramos JD (2017) Effects of silicon on antioxidant enzymes, CO2, proline and biological activity of in vitro-grown cape gooseberry under salinity stress. Australian Journal of Crop Science 11, 438–446.
Effects of silicon on antioxidant enzymes, CO2, proline and biological activity of in vitro-grown cape gooseberry under salinity stress.Crossref | GoogleScholarGoogle Scholar |

Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Frontiers of Plant Science 7, 1–26.
Abscisic acid and abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar |

Schobert B, Tschesche H (1978) Unusual solution properties of proline and its interaction with proteins. Biochimica et Biophysica Acta (BBA) – General Subjects 541, 270–277.
Unusual solution properties of proline and its interaction with proteins.Crossref | GoogleScholarGoogle Scholar |

Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Frontiers of Plant Science 7, 1–21.
Global plant stress signaling: reactive oxygen species at the cross-road.Crossref | GoogleScholarGoogle Scholar |

Shah K, Dubey RS (1997) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biologia Plantarum 40, 121–130.
Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant.Crossref | GoogleScholarGoogle Scholar |

Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD (2011) Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7, 1–6.

Singh D, Laxmi A (2015) Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Frontiers of Plant Science 6, 1–11.
Transcriptional regulation of drought response: a tortuous network of transcriptional factors.Crossref | GoogleScholarGoogle Scholar |

Smrcka AV (2008) G protein βγ subunits: central mediators of G protein-coupled receptor signaling. Cellular and Molecular Life Sciences 65, 2191–2214.
G protein βγ subunits: central mediators of G protein-coupled receptor signaling.Crossref | GoogleScholarGoogle Scholar | 18488142PubMed |

Srivastava U, Singh S, Gautam B, Yadav P, Yadav M, Thomas G, Singh G (2017) Linear epitope prediction in HPV type 16 E7 antigen and their docked interaction with human TMEM 50A structural model. Bioinformation 13, 122–130.
Linear epitope prediction in HPV type 16 E7 antigen and their docked interaction with human TMEM 50A structural model.Crossref | GoogleScholarGoogle Scholar | 28690376PubMed |

Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.

Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signaling & Behavior 2, 135–138.
Abscisic acid and abiotic stress signaling.Crossref | GoogleScholarGoogle Scholar |

Tuteja N (2009) Signaling through G protein-coupled receptors. Plant Signaling & Behavior 4, 942–947.
Signaling through G protein-coupled receptors.Crossref | GoogleScholarGoogle Scholar |

Venekamp JH (1989) Regulation of cytosol acidity in plants under conditions of drought. Physiologia Plantarum 76, 112–117.
Regulation of cytosol acidity in plants under conditions of drought.Crossref | GoogleScholarGoogle Scholar |

Viklund H, Elofsson A (2004) Best α‐helical transmembrane protein topology predictions are achieved using hidden Markov models and evolutionary information. Protein Science 13, 1908–1917.
Best α‐helical transmembrane protein topology predictions are achieved using hidden Markov models and evolutionary information.Crossref | GoogleScholarGoogle Scholar | 15215532PubMed |

Wang W, Xia M, Chen J, Deng F, Yuan R, Zhang X, Shen F (2016) Data set for phylogenetic tree and RAMPAGE Ramachandran plot analysis of SODs in Gossypium raimondii and G. arboreum. Data in Brief 9, 345–348.
Data set for phylogenetic tree and RAMPAGE Ramachandran plot analysis of SODs in Gossypium raimondii and G. arboreum.Crossref | GoogleScholarGoogle Scholar | 27672674PubMed |

Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research 35, W407–W410.
ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins.Crossref | GoogleScholarGoogle Scholar | 17517781PubMed |

Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. The Plant Cell 18, 1310–1326.
Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors.Crossref | GoogleScholarGoogle Scholar | 16603654PubMed |

You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Frontiers of Plant Science 6, 1–15.
ROS regulation during abiotic stress responses in crop plants.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Gao Z, Zheng X, Zhang Z (2012) The role of G-proteins in plant immunity. Plant Signaling & Behavior 7, 1284–1288.
The role of G-proteins in plant immunity.Crossref | GoogleScholarGoogle Scholar |