Abstract
Receptor like kinases (RLKs) are preserved upstream signaling molecules which regulate several biological processes from plant development to various stress adaptation programs. Non arginine aspartate (non-RD) a prominent class of RLKs plays a significant role in disease resistance and apoptosis in plants. In present investigation, a comprehensive in silico analysis for non-RD Kinase gene family as well as identification of gene structures, sequence similarity, chromosomal localization, gene duplication analysis, promoter analysis, transcript expression profiles and phylogenic studies were done. In this study, twenty-six genes were observed on nine out of twelve chromosomes. All these genes were clustered into five subfamilies under large monophyletic group termed as Interleukin-1 Receptor-Associated Kinase (IRAK) family. Some of the important physiochemical properties of twenty-six proteins are determined and ranged in the following order: (a) Amino acids size ranged from (620 to 1781) (b) Molecular weight ranged as of (70.11 to 197.11 KDa) and (c) Theoretical PI ranged from (5.69 to 8.63) respectively. Structural diversity in genomic structure among non-RD kinase gene family was identified and presence of pathogen induced cis regulatory elements including STRE, MYC, MYB, and W box were found. Expression profiles revealed the potential ability of three genes CaRLK1 from LRRXII and CaRLK15,16 from stress antifung subfamily were pointedly upregulated beyond the severe stress time period (9 DAI) in anthracnose resistant genotype PBC-80 in response to Colletotrichum truncatum infection. Subsequently, in silico studies from the available genome sequencing data helped us to identify candidate genes tangled in inducing disease resistance.
Similar content being viewed by others
References
Afzal AJ, Wood AJ, Lightfoot DA (2008) Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant-Microbe Interact 21:507–517. https://doi.org/10.1094/MPMI-21-5-0507
Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A, Wishart DS (2016) Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res 44:147–153. https://doi.org/10.1093/nar/gkw419
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–208. https://doi.org/10.1093/nar/gkp335
Barzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM (2014) New insights into the regulation of aquaporins by the arbuscularmycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant-Microbe Interact 27:349–363. https://doi.org/10.1094/mpmi-09-13-0268-R
Bai Y, Sunarti S, Kissoudis C, Visser RGF, Van Der Linden G (2018) The role of tomato WRKY genes in plant responses to combined abiotic and biotic stresses. Front Plant Sci 9:801. https://doi.org/10.3389/fpls.2018.00801
Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280. https://doi.org/10.1093/nar/30.1.276
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10. https://doi.org/10.1038/s41598-017-17248-7
Chowdhury S, Basu A, Kundu S (2017) Biotrophy-necrotrophy switch in pathogen evokes differential response in resistant and susceptible sesame involving multiple signaling pathways at different phases. Sci Rep 7:17251. https://doi.org/10.1038/s41598-017-17248-7
Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B (2006) AB-lectin receptorkinase gene conferring rice blast resistance. Plant J 46:794–804. https://doi.org/10.1111/j.1365-313X.2006.02739.x
Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction: twenty-something years on. Nat Protoc 1:581–585. https://doi.org/10.1038/nprot.2006.83
Dardick C, Ronald P (2006) Plant and animal pathogen recognition receptors signal through non-RD kinases. PLOS Pathog 2:e2. https://doi.org/10.1371/journal.ppat.0020002
Dardick C, Schwessinger B, Ronald P (2012) Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Curr Opin Plant Boil 15:358–366. https://doi.org/10.1016/j.pbi.2012.05.002
Delteil A, Gobbato E, Cayrol B, Estevan J, Michel-Romiti C, Dievart A, Kroj T, Morel JB (2016) Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol 16:17. https://doi.org/10.1186/s12870-016-0711-x
Diao W, Snyder J, Wang S, Liu J, Pan B, Guo G, Ge W, Dawood M (2018) Genome-wide analyses of the NAC transcription factor gene family in pepper (Capsicum annuum L.): chromosome location, phylogeny, structure, expression patterns, cis-elements in the promoter, and interaction network. Int J Mol Sci 19:1028. https://doi.org/10.3390/ijms19041028
Feng X, Jiang J, Padhi A, Ning C, Fu J, Wang A, Mrode R, Liu JF (2017) Characterization of genome-wide segmental duplications reveals a common genomic feature of association with immunity among domestic animals. BMC Genom 18:293. https://doi.org/10.1186/s12864-017-3690-x
Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F (2006) Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62:305–323. https://doi.org/10.1007/s11103-006-9022-1
Haffani YZ, Silva NF, Goring DR (2004) Receptor kinase signalling in plants. Can J Bot 82:1–5. https://doi.org/10.1139/b03-126
Hofberger JA, Nsibo DL, Govers F, Bouwmeester K, Schranz ME (2015) A complex interplay of tandem-and whole-genome duplication drives expansion of the L-type lectin receptor kinase gene family in the brassicaceae. Genome Biol Evol 7:720–734. https://doi.org/10.1093/gbe/evv020
Huang BH, Chen YW, Huang CL, Gao J, Liao PC (2016) Imbalanced positive selection maintains the functional divergence of duplicated DIHYDROKAEMPFEROL 4-REDUCTASE genes. Sci Rep 6:39031. https://doi.org/10.1038/srep39031
He S (2015) Genome-wide identification and transcriptional expression analysis of mitogen-activated protein kinase and mitogen-activated protein kinase genes in Capsicum annuum. Front Plant Sci 6:780. https://doi.org/10.3389/fpls.2015.00780
Jin B, Sheng Z, Muhammad I, Chen J, Yang H (2019) Cloning and functional analysis of the promoter of a stress-inducible gene (Zmap) in maize. PLoS ONE 14:e0211941. https://doi.org/10.1371/journal.pone.0211941
Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y (2010) Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J 64:343–354. https://doi.org/10.1111/j.1365-313X.2010.04328.x
Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:2163–1498. https://doi.org/10.1093/oxfordjournals.molbev.a026248
Kong W, Ding L, Cheng J, Wang B (2018) Identification and expression analysis of genes with pathogen-inducible cis-regulatory elements in the promoter regions in Oryza sativa. Rice 11:52. https://doi.org/10.1186/s12284-018-0243-0
Letunic I, Doerks T, Bork P (2011) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:302–305. https://doi.org/10.1093/nar/gkr931
Passricha N, Saifi SK, Singh R, Kharb P, Tuteja N (2019) Receptor-like kinases control the development, stress response, and senescence in plants. Senescence signalling and control in plants. Academic Press, New York, pp 199–210
Li J, Hou H, Li X, Xiang J, Yin X, Gao H, Zheng Y, Bassett CL, Wang X (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus× domestica Borkh). Plant Physiol Biochem 70:100–114. https://doi.org/10.1016/j.plaphy.2013.05.021
Liu PL, Huang Y, Shi PH, Yu M, Xie JB, Xie L (2018) Duplication and diversification of lectin receptor-like kinases (LecRLK) genes in soybean. Sci Rep 8:5861. https://doi.org/10.1038/s41598-018-24266-6
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–DDCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Mishra R, Nanda S, Rout E, Chand SK, Mohanty JN, Joshi RK (2017) Differential expression of defense-related genes in chilli pepper infected with anthracnose pathogen Colletotrichum truncatum. Physiol Mol Plant Pathol 97:1–10. https://doi.org/10.1016/j.pmpp.2016.11.001
Petersen TN, Brunak S, Von Heijne G, Nielsen H (2011) Signal P 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785. https://doi.org/10.1038/nmeth.1701
Qi PF, Johnston A, Balcerzak M, Rocheleau H, Harris LJ, Long XY, Wei YM, Zheng YL, Ouellet T (2012) Effect of salicylic acid on Fusarium graminearum, the major causal agent of fusarium head blight in wheat. Fungal Biol 116:413–426. https://doi.org/10.1016/j.funbio.2012.01.001
Qin L, Mo N, Muhammad T, Liang Y (2018) Genome-wide analysis of DCL, AGO, and RDR gene families in Hot pepper (Capsicum annuumL.). Int. J. Mol Sci 19:1038. https://doi.org/10.3390/ijms19041038
Ridzuan R, Rafii M, Ismail S, Mohammad Yusoff M, Miah G, Usman M (2018) Breeding for anthracnose disease resistance in chili: progress and prospects. Int J Mol Sci 19:3122. https://doi.org/10.3390/ijms19103122
Roy CB, Liu H, Rajamani A, Saha T (2019) Transcriptome profiling reveals genetic basis of disease resistance against Corynespora cassiicola in rubber tree (Hevea brasiliensis). Curr Plant Biol 17:2–16
Raj TS, Christopher DJ (2009) Effect of bio-control agents and fungicides against Colletotrichum capsici causing fruit rot of chilli. Ann Plant Protect Sci 17:143–145. https://doi.org/10.5897/AJB2013.13558
Saijo Y, Loo EPI, Yasuda S (2018) Pattern recognition receptors and signaling in plant–microbe interactions. Plant J 39:592–613. https://doi.org/10.1111/tpj.13808
Sakamoto T, Deguchi M, Brustolini OJ, Santos AA, Silva FF, Fontes EP (2012) The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol 12(1):229
Saxena A, Raghuwanshi R, Singh HB (2018) Molecular, phenotypic and pathogenic variability in Colletotrichum isolates of subtropical region in north-eastern India, causing fruit rot of chillies. J Appl Microbiol 117:1422–1434. https://doi.org/10.1111/jam.12607
Saxena A, Raghuwanshi R, Gupta VK, Singh HB (2016) Chilli anthracnose: the epidemiology and management. Front Microbiol 7:1527. https://doi.org/10.3389/fmicb.2016.01527
Singh P, Kuo YC, Mishra S, Tsai CH, Chien CC, Chen CW, Desclos-Theveniau M, Chu PW, Schulze B, Chinchilla D, Boller T (2012) The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity. Plant Cell 24:12561270. https://doi.org/10.1105/tpc.112.095778
Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast-online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 15(44):W232–235. https://doi.org/10.1093/nar/gkw256
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Wang Y, Liu J, Huang BO, Xu YM, Li J, Huang LF, Lin J, Zhang J, Min QH, Wang YWM (2015) Mechanism of alternative splicing and its regulation. Biomed Rep 3:152–158. https://doi.org/10.3892/br.2014.407
Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon–intron structure. PNAS 109:1187–1192
Xu Z, Gao L, Tang M, Qu C, Huang J, Wang Q, Yang C, Liu G, Yang C (2017) Genome-wide identification and expression profile analysis of CCH gene family in populous. PeerJ 5:e3962. https://doi.org/10.7717/peerj.3962
Yang X, Jawdy S, Tschaplinski TJ, Tuskan GA (2009) Genome-wide identification of lineage-specific genes in Arabidopsis, Oryza and Populus. Genomics 93:473–480. https://doi.org/10.1016/j.ygeno.2009.01.002
Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760. https://doi.org/10.1016/j.cell.2006.03.037
Acknowledgement
Authors were thankful to Head of the department and Co-scholars of bioinformatics lab for providing facilities to carry out the work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors do not have any conflict of interest to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Srideepthi, R., Krishna, M.S.R., Suneetha, P. et al. Genome-wide identification, characterization and expression analysis of non-RD receptor like kinase gene family under Colletotrichum truncatum stress conditions in hot pepper. Genetica 148, 283–296 (2020). https://doi.org/10.1007/s10709-020-00104-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-020-00104-4