Transcriptome-Wide Identification of Nine Tandem Peptide Repeat Families in Roselle (Hibiscus sabdariffa L.)
Main Article Content
Abstract
Plants are rich in tandem repeats-containing proteins. It is postulated that the occurrence of tandem repeat gene families facilitates the adaptation and survival of plants in adverse environmental conditions. This study intended to identify the tandem repeats in the transcriptome of a high potential tropical horticultural plant, roselle (Hibiscus sabdariffa L.). A total of 92,974 annotated de novo assembled transcripts were analysed using in silico approach, and 6,541 transcripts that encoded proteins containing tandem repeats with length of 20–60 amino acid residues were identified. Domain analysis revealed a total of nine tandem repeat protein families in the transcriptome of roselle, which are the Ankyrin repeats (ANK), Armadillo repeats (ARM), elongation factor-hand domain repeats (EFhand), Huntingtin, elongation factor 3, protein phosphatase 2A, yeast kinase TOR1 repeats (HEAT), Kelch repeats (Kelch), leucine rich repeats (LRR), pentatricopeptide repeats (PPR), tetratricopeptide repeats (TPR) and WD40 repeats (WD40). Functional annotation analysis further matched 6,236 transcripts to 1,045 known proteins that contained tandem repeats including proteins implicated in plant development, protein-protein interaction, immunity and abiotic stress responses. The findings provide new insights into the occurrence of tandem repeats in the transcriptome and lay the foundation to elucidate the functional associations between tandem peptide repeats (TRs) and proteins in roselle and facilitate the identification of novel biotic and abiotic response related tandem repeats genes that may be useful in breeding improved varieties.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Afzal A J, Wood A J and Lightfoot D A. (2008). Plant receptor-like serine threonine kinases: Roles in signaling and plant defense. Molecular Plant Microbe Interactions 21(5): 507–517. https://doi.org/10.1094/MPMI-21-5-0507
Bairoch A and Apweiler R. (2000). The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Research 28(1): 45–48. https://doi.org/10.1093/nar/28.1.45
Barkan A and Small I. (2014). Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology 65: 415–442. https://doi.org/10.1146/annurevarplant-050213-040159
Baruah A, Šimková K, Hincha D K, Apel K and Laloi C. (2009). Modulation of 1O2-mediated retrograde signaling by the pleiotropic response locus 1 (PRL1) protein, a central integrator of stress and energy signaling. The Plant Journal 60(1): 22–32. https://doi.org/10.1111/j.1365-313X.2009.03935.x
Becerra C, Jahrmann T, Puigdomènech P and Vicient C M. (2004). Ankyrin repeat containing proteins in Arabidopsis: Characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. Gene 340(1): 111–121. https://doi.org/10.1016/j.gene.2004.06.006
Binder B M, Walker J M, Gagne J M, Emborg T J, Hemmann G, Bleecker A B and Vierstra R D. (2007). The Arabidopsis EIN3 binding F-Box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 19(2): 509–523. https://doi.org/10.1105/tpc.106.048140
Bittner-Eddy P D, Crute I R, Holub E B and Beynon J L. (2000). RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. The Plant Journal 21(2): 177–188. https://doi.org/10.1046/j.1365-313x.2000.00664.x
Boonburapong B and Buaboocha T. (2007) Genome-wide identification and analyses of the rice calmodulin and related potential calcium sensor proteins. BMC Plant Biology 7: 4. https://doi.org/10.1186/1471-2229-7-4
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K and Madden T L. (2009). BLAST+: Architecture and applications. BMC Bioinformatics 10: 421. https://doi.org/10.1186/1471-2105-10-421
Canonne J, Froidure-Nicolas S and Rivas S. (2011). Phospholipases in action during plant defense signaling. Plant Signaling and Behavior 6(1): 13–18. https://doi.org/10.4161/psb.6.1.14037
Cao H, Glazebrook J, Clarke J D, Volko S and Dong X. (1997). The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88(1): 57–63. https://doi.org/10.1016/s0092-8674(00)81858-9
Chakraborty S, Nguyen B, Wasti S D and Xu G. (2019). Plant leucine-rich repeat receptor kinase (LRR-RK): Structure, ligand perception, and activation mechanism. Molecules 24(17): 3081. https://doi.org/10.3390/molecules24173081
Chen G, Zou Y, Hu J and Ding Y. (2018). Genome-wide analysis of the rice PPR gene family and their expression profiles under different stress treatments. BMC Genomics 19: 720. https://doi.org/10.1186/s12864-018-5088-9
Chen T H, Sotomayor M and Gopalan V. (2019). Biochemical studies provide insights into the necessity for multiple Arabidopsis thaliana protein-only RNase P isoenzymes. Journal of Molecular Biology 431(3): 615–624. https://doi.org/10.1016/j.jmb.2018.11.004
Cid-Ortega S and Guerrero-Beltrán J A. (2015). Roselle calyces (Hibiscus sabdariffa), an alternative to the food and beverages industries: A review. The Journal of Food Science and Technology 52: 6859–6869. https://doi.org/10.1007/s13197-015-1800-9
Colcombet J, Lopez Obando M, Heurtevin L, Bernard C, Martin K, Berthomé R and Lurin C. (2013). Systematic study of subcellular localization of Arabidopsis PPR proteins confirms a massive targeting to organelles. RNA Biology 10(9): 1557–1575. https://doi.org/10.4161/rna.26128
Collins J, O’Grady K, Chen S and Gurley W. (2019). The C-terminal WD40 repeats on the TOPLESS co-repressor function as a protein–protein interaction surface. Plant Molecular Biology 100(1): 47–58. https://doi.org/10.1007/s11103-019-00842-w
Da-Costa-Rocha I, Bonnlaender B, Sievers H, Pischel I and Heinrich M. (2014). Hibiscus sabdariffa L.: A phytochemical and pharmacological review. Food Chemistry 165: 424–443. https://10.1016/j.foodchem.2014.05.002
Day I S, Reddy V S, Shad Ali G and Reddy A S N. (2002). Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biology 3: research0056.1. https://doi.org/10.1186/gb-2002-3-10-research0056
de Longevialle A F, Hendrickson L, Taylor N L, Delannoy E, Lurin C, Badger M, Millar A H and Small I. (2008). The pentatricopeptide repeat gene OTP51 with two LAGLIDADG motifs is required for the cis-splicing of plastid ycf3 intron 2 in Arabidopsis thaliana. The Plant Journal 56(1): 157–168. https://doi.org/10.1111/j.1365-313X.2008.03581.x
Delucchi M, Schaper E, Sachenkova O, Elofsson A and Anisimova M. (2020). A new census of protein tandem repeats and their relationship with intrinsic disorder. Genes 11(4): 407. https://doi.org/10.3390/genes11040407
Despres B, Delseny M and Devic M. (2001). Partial complementation of embryo defective mutations: A general strategy to elucidate gene function. The Plant Journal 27(2): 149–159. https://doi.org/10.1046/j.1365-313x.2001.01078.x
DeYoung B J and Innes R W. (2006). Plant NBS-LRR proteins in pathogen sensing and host defense. Nature Immunology 7(12): 1243–1249. https://doi.org/10.1038/ni1410
Dinesh D C, Villalobos L I A C and Abel S. (2016). Structural biology of nuclear auxin action. Trends in Plant Science 21(4): 302–316. https://doi.org/10.1016/j.tplants.2015.10.019
Dufayard J F, Bettembourg M, Fischer I, Droc G, Guiderdoni E, Périn C, Chantret N and Diévart A. (2017). New insights on leucine-rich repeats receptor-like kinase orthologous relationships in angiosperms. Frontiers of Plant Science 8: 381. https://doi.org/10.3389/fpls.2017.00381
Feng L, Gao Z, Xiao G, Huang R and Zhang H. (2014). Leucine-rich repeat receptor-like kinase FON1 regulates drought stress and seed germination by activating the expression of ABA-responsive genes in rice. Plant Molecular Biology Reporter 32: 1158–1168. https://doi.org/10.1007/s11105-014-0718-0
Fernández-Bautista N, Fernández-Calvino L, Muñoz A, Toribio R, Mock H P and Castellano M M. (2018). HOP family plays a major role in long-term acquired thermotolerance in Arabidopsis. Plant Cell and Environment 41(8): 1852–1869. https://doi.org/10.1111/pce.13326
Finn R D, Bateman A, Clement J, Coggill P, Eberhardt R Y, Eddy S R, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer E L L, Tate J and Punta M. (2014). Pfam: The protein families database. Nucleic Acids Research 42(D1): D222–D230. https://doi.org/10.1093/nar/gkt1223
Finn R D, Clements J and Eddy S R. (2011). HMMER web server: Interactive sequence similarity searching. Nucleic Acids Research 39(Suppl. 2): W29–37. https://doi.org/10.1093/nar/gkr367
Friedrichsen D M, Joazeiro C A P, Li J, Hunter T and Chory J. (2000). Brassinosteroidinsensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiology 123(4): 1247–1256. https://doi.org/10.1104/pp.123.4.1247
Gao C, Sun P, Wang W and Tang D. (2021). Arabidopsis E3 ligase KEG associates with and ubiquitinates MKK4 and MKK5 to regulate plant immunity. Journal of Integrative Plant Biology 63(2): 327–339. https://doi.org/10.1111/jipb.13007
Gottin C, Dievart A, Summo M, Droc G, Périn C, Ranwez V and Chantret N. (2021). A new comprehensive annotation of leucine-rich repeat-containing receptors in rice. The Plant Journal 108(2): 492–508. https://doi.org/10.1111/tpj.15456
Gutmann B, Royan S, Schallenberg-Rüdinger M, Lenz H, Castleden I R, McDowell R, Vacher M A et al. (2020). The expansion and diversification of pentatricopeptide repeat RNA-editing factors in plants. Molecular Plant 13(2): 215–230. https://doi.org/10.1016/j.molp.2019.11.002
Haas B J, Papanicolaou A, Yassour M, Grabherr M, Blood P D, Bowden J, Couger M B et al. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocol 8: 1494–1512. https://doi.org/10.1038/nprot.2013.084
Hacquard T, Clavel M, Baldrich P, Lechner E, Pérez-Salamó I, Schepetilnikov M, Derrien B, et al. (2022). The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA. Cell Reports 39(2): 110671. https://doi.org/10.1016/j.celrep.2022.110671
Hammani K, Gobert A, Hleibieh K, Choulier L, Small I and Giegé P. (2011). An Arabidopsis dual-localized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation. Plant Cell 23(2): 730–740. https://doi.org/10.1105/tpc.110.081638
Hamzah N A, Yong C S Y and Nallappan M. (2022). The first transcriptome dataset of roselle (Hibiscus sabdariffa L.) calyces during maturation. Data in Brief 45: 108613. https://doi.org/10.1016/j.dib.2022.108613
Hayes M L, Giang K, Berhane B and Mulligan R M. (2013). Identification of two pentatricopeptide repeat genes required for RNA editing and zinc binding by C-terminal cytidine deaminase-like domains. Journal of Biological Chemistry 288(51): 36519–36529. https://doi.org/10.1074/jbc.M113.485755
Hong M J, Kim J B, Seo Y W and Kim D Y. (2021). Regulation of glycosylphosphatidylinositol-anchored protein (GPI-AP) expression by F-Box/LRR-Repeat (FBXL) protein in wheat (Triticum aestivum L.). Plants 10(8): 1606. https://doi.org/10.3390/plants10081606
Huang J, Zhao X, Yu H, Ouyang Y, Wang L and Zhang Q. (2009). The ankyrin repeat gene family in rice: Genome-wide identification, classification and expression profiling. Plant Molecular Biology 71(3): 207–226. https://doi.org/10.1007/s11103-009-9518-6
Hwang S G, Kim D S and Jang C S. (2011). Comparative analysis of evolutionary dynamics of genes encoding leucine-rich repeat receptor-like kinase between rice and Arabidopsis. Genetica 139: 1023–1032. https://doi.org/10.1007/s10709-011-9604-y
Ikeda M, Mitsuda N and Ohme-Takagi M. (2009). Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21(11): 3493–3505. https://doi.org/10.1105/tpc.109.069997
Jamini T S and Aminul-Islam A K M. (2021). Roselle (Hibiscus sabdariffa L.): Nutraceutical and pharmaceutical significance. In S M Sapuan, R Nadlene, A M Radzi and R A Ilyas (eds.). Roselle: Production, processing, products and biocomposites. Cambridge, UK: Academic Press, 103–119. https://doi.org/10.1016/B978-0-323-85213-5.00001-9
Jernigan K K and Bordenstein S R. (2015). Tandem-repeat protein domains across the tree of life. PeerJ: Life and Environment 3: e732. https://doi.org/10.7717/peerj.732
Johnson X, Wostrikoff K, Finazzi G, Kuras R, Schwarz C, Bujaldon S, Nickelsen J, Stern D B, Wollman F A and Vallon O. (2010). MRL1, a conserved pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell 22(1): 234–248. https://doi.org/10.1105/tpc.109.066266
Jones D S, John A, VanDerMolen K R and Nimchuk Z L. (2021). CLAVATA signaling ensures reproductive development in plants across thermal environments. Current Biology 31(1): 220–227. https://doi.org/10.1016/j.cub.2020.10.008
Jose J, Ghantasala S and Choudhury R S. (2020). Arabidopsis transmembrane receptor-like kinases (RLKs): A bridge between extracellular signal and intracellular regulatory machinery. International Journal of Molecular Sciences 21(11): 4000. https://doi.org/10.3390/ijms21114000
Kruijt M, de Kock M J D and de Wit P J G M. (2005). Receptor-like proteins involved in plant disease resistance. Molecular Plant Pathology 6(1): 85–97. https://doi.org/10.1111/j.1364-3703.2004.00264.x
Kurek I, Aviezer K, Erel N, Herman E and Breiman A. (1999). The wheat peptidyl prolyl cistrans- isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiology 119(2): 693–704. https://doi.org/10.1104/pp.119.2.693
Lai S H and Chye M L. (2021). Plant acyl-coa-binding proteins—Their lipid and protein interactors in abiotic and biotic stresses. Cells 10(5): 1064. https://doi.org/10.3390/cells10051064
Lakhssassi N, Liu S M, Bekal S, Zhou Z, Colantonio V, Lambert K, Berakat A and Meksem K. (2017). Characterization of the soluble NSF attachment protein gene family identifies two members involved in additive resistance to a plant pathogen. Scientific Reports 7: 45226. https://doi.org/10.1038/srep45226
Laluk K, Abuqamar S and Mengiste T. (2011). The Arabidopsis mitochondria-localized pentatricopeptide repeat protein PGN functions in defense against necrotrophic fungi and abiotic stress tolerance. Plant Physiology 156(4): 2053–2068. https://doi.org/10.1104/pp.111.177501
Langmead B and Salzberg S L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods 9(4): 357–359. https://doi.org/10.1038/nmeth.1923
Le M H, Cao Y, Zhang X C and Stacey G. (2014). LIK1, a CERK1-interacting kinase, regulates plant immune responses in Arabidopsis. PLoS ONE 9(7): e102245. https://doi.org/10.1371/journal.pone.0102245
Lechner E, Achard P, Vansiri A, Potuschak T and Genschik P. (2006). F-box proteins everywhere. Current Opinion in Plant Biology 9(6): 631–638. https://doi.org/10.1016/j.pbi.2006.09.003
Lee H A and Yeom S I. (2015). Plant NB-LRR proteins: Tightly regulated sensors in a complex manner. Briefings in Functional Genomics 14(4): 233–242. https://doi.org/10.1093/bfgp/elv012
Lermontova I, Fuchs J and Schubert I. (2008). The Arabidopsis checkpoint protein Bub3.1 is essential for gametophyte development. Frontiers in Bioscience 13(13): 5202–5211. https://doi.org/10.2741/3076
Leung K C, Li H Y, Mishra G and Chye M L. (2004). ACBP4 and ACBP5, novel Arabidopsis acyl-CoA-binding proteins with Kelch motifs that bind oleoyl-CoA. Plant Molecular Biology 55(2): 297–309. https://doi.org/10.1007/s11103-004-0642-z
Li X, Salman A, Guo C, Yu J, Cao S, Gao X, Li W, Li H and Guo Y. (2018). Identification and characterization of LRR-RLK family genes in potato reveal their involvement in peptide signaling of cell fate decisions and biotic/abiotic stress responses. Cells 7(9): 120. https://doi.org/10.3390/cells7090120
Li X, Sun M, Liu S, Teng Q, Li S and Jiang Y. (2021). Functions of PPR proteins in plant growth and development. International Journal of Molecular Sciences 22(20): 11274. https://doi.org/10.3390/ijms222011274
Li Z, Wang Y, Huang J, Ahsan N, Biener G, Paprocki J, Thelen J J, Raicu V and Zhao D. (2017). Two SERK receptor-like kinases interact with EMS1 to control anther cell fate determination. Plant Physiology 173(1): 326–337. https://doi.org/10.1104/pp.16.01219
Liao Y, Hu C, Zhang X, Cao X, Xu Z, Gao X, Li L, Zhu J and Chen R. (2017). Isolation of a novel leucine-rich repeat receptor-like kinase (OsLRR2) gene from rice and analysis of its relation to abiotic stress responses. Biotechnology and Biotechnological Equipment 31(1): 51–57. https://doi.org/10.1080/13102818.2016.1242377
Liu P L, Du L, Huang Y, Gao S M and Yu M. (2017). Origin and diversification of leucine-rich repeat receptor-like protein kinase (LRR-RLK) genes in plants. BMC Evolutionary Biology 17(1): 47. https://doi.org/10.1186/s12862-017-0891-5
Liu Y, Sun T, Sun Y, Zhang Y, Radoji?i? A, Ding Y, Tian H et al. (2020). Diverse roles of the salicylic acid receptors NPR1 and NPR3/NPR4 in plant immunity. Plant Cell 32(12): 4002–4016. https://doi.org/10.1105/tpc.20.00499
Lu H, Rate D N, Song J T and Greenberg J T. (2003). ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15(10): 2408–2420. https://doi.org/10.1105/tpc.015412
Luo H and Nijveen H. (2014). Understanding and identifying amino acid repeats. Briefings in Bioinformatics 15(4): 582–591. https://doi.org/10.1093/bib/bbt003
Luptov?iak I, Komis G, Taká? T, Ove?ka M and Šamaj J. (2017). Katanin: A sword cutting microtubules for cellular, developmental, and physiological purposes. Frontiers of Plant Science. 8: 1982. https://doi.org/10.3389/fpls.2017.01982
Marone D, Russo M A, Laidò G, De Leonardis A M and Mastrangelo A M. (2013). Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: Active guardians in host defense responses. International Journal of Molecular Sciences 14(4): 7302–7326. https://doi.org/10.3390/ijms14047302
Martin-Arevalillo R, Nanao M H, Larrieu A, Vinos-Poyo T, Mast D, Galvan-Ampudia C, Brunoud G, Vernoux T, Dumas R and Parcy F. (2017). Structure of the Arabidopsis TOPLESS corepressor provides insight into the evolution of transcriptional repression. The Proceedings of the National Academy of Sciences 114(30): 8107–8112. https://doi.org/10.1073/pnas.1703054114
McHale L, Tan X, Koehl P and Michelmore R W. (2006). Plant NBS-LRR proteins: Adaptable guards. Genome Biology 7: 212. https://doi.org/10.1186/gb-2006-7-4-212
Mehdi S, Derkacheva M, Ramström M, Kralemann L, Bergquist J and Hennig L. (2016). The WD40 domain protein MSI1 functions in a histone deacetylase complex to fine-tune abscisic acid signaling. Plant Cell 28(1): 42–54. https://doi.org/10.1105/tpc.15.00763
Mishra A K, Puranik S and Prasad M. (2012). Structure and regulatory networks of WD40 protein in plants. Journal of Plant Biochemistry Biotechnology 21(1): 32–39. https://doi.org/10.1007/s13562-012-0134-1
Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, Shinozaki K and Yamaguchi-Shinozaki K. (2007). Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. The Plant Journal 50(5): 751–766. https://doi.org/10.1111/j.1365-313X.2007.03083.x
Mohr T J, Mammarella N D, Hoff T, Woffenden B J, Jelesko J G and McDowell J M. (2010). The Arabidopsis downy mildew resistance gene RPP8 is induced by pathogens and salicylic acid and is regulated by W box cis elements. Molecular Plant Microbe Interactions 10: 1303–1315. https://doi.org/10.1094/MPMI-01-10-0022
Morales-Luna E, Pérez-Ramírez I F, Salgado L M, Castaño-Tostado E, Gómez-Aldapa C A and Reynoso-Camacho R. (2019). The main beneficial effect of roselle (Hibiscus sabdariffa) on obesity is not only related to its anthocyanin content. Journal of the Science of Food and Agriculture 99(2): 596–605. https://doi.org/10.1002/jsfa.9220
Morillo S A and Tax F E. (2006). Functional analysis of receptor-like kinases in monocots and dicots. Current Opinion in Plant Biology 9(5): 460–469. https://doi.org/10.1016/j.pbi.2006.07.009
Mudgil Y, Shiu S H, Stone S L, Salt J N and Goring D R. (2004). A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family. Plant Physiology 134(1): 59–66. https://doi.org/10.1104/pp.103.029553
Nakamura T, Yagi Y and Kobayashi K. (2012). Mechanistic insight into pentatricopeptide repeat proteins as sequence-specific RNA-binding proteins for organellar RNAs in plants. Plant and Cell Physiology 53(7): 1171–1179. https://doi.org/10.1093/pcp/pcs069
Navarro C, Moore J, Ott A, Baumert E, Mohan A, Gill K S and Sandhu D. (2015). Evolutionary, comparative and functional analyses of the Brassinosteroid receptor gene, BRI1, in wheat and its relation to other plant genomes. PLoS One 10(5): e0127544. https://doi.org/10.1371/journal.pone.0127544
Ng A and Xavier R J. (2011). Leucine-rich repeat (LRR) proteins: Integrators of pattern recognition and signaling in immunity. Autophagy 7(9): 1082–1084. https://doi.org/10.4161/auto.7.9.16464
Nithianantharajah J and Hannan A J. (2007). Dynamic mutations as digital genetic modulators of brain development, function and dysfunction. BioEssays 29(6): 525–535. https://doi.org/10.1002/bies.20589
Ouyang Y, Huang X, Lu Z and Yao J. (2012). Genomic survey, expression profile and coexpression network analysis of OsWD40 family in rice. BMC Genomics 13: 100. https://doi.org/10.1186/1471-2164-13-100
Padmanabhan M, Cournoyer P and Dinesh-Kumar S P. (2009). The leucine-rich repeat domain in plant innate immunity: A wealth of possibilities. Cellular Microbiology 11(2): 191–198. https://doi.org/10.1111/j.1462-5822.2008.01260.x
Pandey G K, Kanwar P, Singh A, Steinhorst L, Pandey A, Yadav A K, Tokas I, et al. (2015). Calcineurin B-like protein-interacting protein kinase CIPK21 regulates osmotic and salt stress responses in Arabidopsis. Plant Physiology 169(1): 780–792. https://doi.org/10.1104/pp.15.00623
Parra R G, Espada R, Verstraete N and Ferreiro D U. (2015). Structural and energetic characterization of the ankyrin repeat protein family. PLoS Computational Biology 11(12): e1004659. https://doi.org/10.1371/journal.pcbi.1004659
Peart J R, Lu R, Sadanandom A, Malcuit I, Moffett P, Brice D C, Schauser L, et al. (2002). Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. The Proceedings of the National Academy of Sciences 99(16): 10865–10869. https://doi.org/10.1073/pnas.152330599
Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X, Ma Q, Zhu S and Cheng B. (2012). CCCH-type zinc finger family in maize: Genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS ONE 7(7): e40120. https://doi.org/10.1371/journal.pone.0040120
Pillitteri L J and Torii K U. (2012). Mechanisms of stomatal development. Annual Review of Plant Biology 63: 591–614. https://doi.org/10.1146/annurevarplant-042811-105451
Qu K, Wei L, Yu J and Wang C. (2019). Identifying plant pentatricopeptide repeat coding gene/protein using mixed feature extraction methods. Frontiers of Plant Science 9: 1–10. https://doi.org/10.3389/fpls.2018.01961
Ren R C, Wang L L, Zhang L, Zhao Y J, Wu J W, Wei Y M, Zhang X S and Zhao X Y. (2020). DEK43 is a P-type pentatricopeptide repeat (PPR) protein responsible for the Cissplicing of nad4 in maize mitochondria. Journal of Integrative Plant Biology 62(3): 299–313. https://doi.org/10.1111/jipb.12843
Riaz G and Chopra R. (2018). A review on phytochemistry and therapeutic uses of Hibiscus sabdariffa L. Biomedicine and Pharmacotherapy 102: 575–586. https://doi.org/10.1016/j.biopha.2018.03.023
Rosado A, Schapire A L, Bressan R A, Harfouche A L, Hasegawa P M, Valpuesta V and Botella M A. (2006). The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity1. Plant Physiology 142(3): 1113–1126. https://doi.org/10.1104/pp.106.085191
Sakamoto H, Matsuda O and Iba K. (2008). ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in salt-stress tolerance in Arabidopsis thaliana. The Plant Journal 56(3): 411–422. https://doi.org/10.1111/j.1365-313X.2008.03614.x
Saleme M L S, Rocha I A and Eloy N B. (2021). The role of anaphase-promoting complex/cyclosome (APC/C) in plant reproduction. Frontiers of Plant Science 12: 642934. https://doi.org/10.3389/fpls.2021.642934
Schaper E and Anisimova M. (2015). The evolution and function of protein tandem repeats in plants. New Phytologist 206(1): 397–410. https://doi.org/10.1111/nph.13184
Shao Z Q, Xue J Y, Wu P, Zhang Y M, Wu Y, Hang Y Y, Wang B and Chen J Q. (2016). Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiology 170(4): 2095–2109. https://doi.org/10.1104/pp.15.01487
Sharma A D, Wajapeyee N, Yadav V and Singh P. (2003). Stress-induced changes in peptidyl-prolyl cis-trans isomerase activity of Sorghum bicolor seedlings. Biologia Plantatarum 47: 367–371. https://doi.org/10.1023/B:BIOP.0000023879.74558.48
Sharma M and Pandey G K. (2016). Expansion and function of repeat domain proteins during stress and development in plants. Frontiers of Plant Science 6: 1–15. https://doi.org/10.3389/fpls.2015.01218
Sharma M, Singh A, Shankar A, Pandey A, Baranwal V, Kapoor S, Tyagi A K and Pandey G K. (2014). Comprehensive expression analysis of rice Armadillo gene family during abiotic stress and development. DNA Research 21(3): 267–283. https://doi.org/10.1093/dnares/dst056
Shi S, Li S, Asim M, Mao J, Xu D, Ullah Z, Liu G, Wang Q and Liu H. (2018). The Arabidopsis calcium dependent protein kinases (CDPKs) and their roles in plant growth regulation and abiotic stress responses. International Journal of Molecular Sciences 9(7): 1900. https://doi.org/10.3390/ijms19071900
Shiu S H, Karlowski W M, Pan R, Tzeng Y H, Mayer K F X and Li W H. (2004). Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16(5): 1220–1234. https://doi.org/10.1105/tpc.020834
Shpak E D. (2013). Diverse roles of ERECTA family genes in plant development. Journal of Integrative Plant Biology 55(12): 1238–1250. https://doi.org/10.1111/jipb.12108
Shu K and Yang W. (2017). E3 ubiquitin ligases: Ubiquitous actors in plant development and abiotic stress responses. Plant and Cell Physiology 58(9): 1461–1476. https://doi.org/10.1093/pcp/pcx071
Sitaraman J, Bui M and Liu Z. (2008). LEUNIG_HOMOLOG and LEUNIG perform partially redundant functions during Arabidopsis embryo and floral development. Plant Physiology 147(2): 672–681. https://doi.org/10.1104/pp.108.115923
Soltabayeva A, Dauletova N, Serik S, Sandybek M, Omondi J O, Kurmanbayeva A and Srivastava S. (2022). Receptor-like kinases (LRR-RLKs) in response of plants to biotic and abiotic stresses. Plants 11(19): 2660. https://doi.org/10.3390/plants11192660
Sun Y, Zhou X and Ma H. (2007). Genome-wide analysis of Kelch repeat-containing F-box family. Journal of Integrative Plant Biology 49(6): 940–952. https://doi.org/10.1111/j.1744-7909.2007.00498.x
Taká? T, Šamajová O, Pechan T, Luptov?iak I and Šamaj J. (2017). Feedback microtubule control and microtubule-actin crosstalk in Arabidopsis revealed by integrative proteomic and cell biology analysis of KATANIN 1 mutants. Molecular and Cellular Proteomics 16(9): 1591–1609. https://doi.org/10.1074/mcp.M117.068015
Tao Y, Yuan F, Leister R T, Ausubel F M and Katagiri F. (2000). Mutational analysis of the Arabidopsis nucleotide binding site-leucine-rich repeat resistance gene RPS2. Plant Cell 12(12): 2541–2554. https://doi.org/10.1105/tpc.12.12.2541
Toribio R, Mangano S, Fernández-Bautista N, Muñoz A and Castellano M M. (2020). HOP, a co-chaperone involved in response to stress in plants. Frontiers of Plant Science 11: 1–8. https://doi.org/10.3389/fpls.2020.591940
van Nocker S and Ludwig P. (2003). The WD-repeat protein superfamily in Arabidopsis: Conservation and divergence in structure and function. BMC Genomics 4(1): 50. https://doi.org/10.1186/1471-2164-4-50
Von Dentz K E, Silva B S, Queiroz E A I F, Bomfim G F, Nascimento A F, Sugizaki M M and Luvizotto R A M. (2021). Hibiscus sabdariffa ethanolic extract modulates adipokine levels, decreases visceral fat and improves glycemic profile in high-fat/sugar diet-induced obese rats. Nutrition and Food Science 51(2): 222–233. https://doi.org/10.1108/NFS-03-2020-0092
Wang H, Ding Z, Gou M, Hu J, Wang Y, Wang L, Wang Y et al. (2021). Genome-wide identification, characterization, and expression analysis of tea plant autophagyrelated genes (CsARGs) demonstrates that they play diverse roles during development and under abiotic stress. BMC Genomics 22(1): 121. https://doi.org/10.1186/s12864-021-07419-2
Wan H, Yuan W, Ye Q, Wang R, Ruan M, Li Z, Zhou G et al. (2012). Analysis of TIR- and non-TIR-NBS-LRR disease resistance gene analogous in pepper: Characterization, genetic variation, functional divergence and expression patterns. BMC Genomics 13: 502. https://doi.org/10.1186/1471-2164-13-502
Wang X, An Y, Xu P and Xiao J. (2021). Functioning of PPR proteins in organelle RNA metabolism and chloroplast biogenesis. Frontiers of Plant Science 12: 627501. https://doi.org/10.3389/fpls.2021.627501
Wei K and Han P. (2017). Comparative functional genomics of the TPR gene family in Arabidopsis, rice and maize. Molecular Breeding 37: 152. https://doi.org/10.1007/s11032-017-0751-4
Wirthmueller L, Roth C, Banfield M J and Wiermer M. (2013). Hop-on hop-off: Importin-?-guided tours to the nucleus in innate immune signaling. Frontiers of Plant Science 4: 1–8. https://doi.org/10.3389/fpls.2013.00149
Wu Y, Xun Q, Guo Y, Zhang J, Cheng K, Shi T, He K, Hou S, Gou X and Li J. (2016). Genome-wide expression pattern analyses of the Arabidopsis leucine-rich repeat receptor-like kinases. Molecular Plant 9(2): 289–300. https://doi.org/10.1016/j.molp.2015.12.011
Wulff B B, Chakrabarti A and Jones D A. (2009). Recognitional specificity and evolution in the tomato-Cladosporium fulvum pathosystem. Molecular Plant Microbe Interaction 22: 1191–1202. https://doi.org/10.1094/MPMI-22-10-1191
Xiong Q, Li W, Li P, Yang M, Wu C and Eichinger L. (2019). The role of ATG16 in autophagy and the ubiquitin proteasome system. Cells 8(1): 2. https://doi.org/10.3390/cells8010002
Yu S, Ali J, Zhou S, Ren G, Xie H, Xu J, Yu X et al. (2022). From Green Super Rice to green agriculture: Reaping the promise of functional genomics research. Molecular Plant 15(1): 9–26. https://doi.org/10.1016/j.molp.2021.12.001
Yuan X, Zhang S, Qing X, Sun M, Liu S, Su H, Shu H and Li X. (2013). Superfamily of ankyrin repeat proteins in tomato. Gene 523(2): 126–136. https://doi.org/10.1016/j.gene.2013.03.122
Zeng H, Zhang Y, Zhang X, Pi E and Zhu Y. (2017). Analysis of EF-hand proteins in soybean genome suggests their potential roles in environmental and nutritional stress signaling. Frontiers of Plant Science 8: 877. https://doi.org/10.3389/fpls.2017.00877
Zhang Q, Wang Y, Wei H, Fan W, Xu C and Li T. (2021). CCR-NB-LRR proteins MdRNL2and MdRNL6 interact physically to confer broad-spectrum fungal resistance in apple (Malus × domestica). The Plant Journal 108(5): 1522–1538. https://doi.org/10.1111/tpj.15526