Skip to main content
Log in

Genome-Wide Identification and Characterization of CHROMO Domain Family Genes Reveal Roles of the Maize Genes in Heat Stress Response

  • GENETICS
  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

CMT2 and cpSRP43 are key factors in tolerance to heat stress, which have been revealed in Arabidopsis. It is largely unknown whether they play similar roles in heat stress resistance in monocotyledon species. Here we carried out genome-enabled identification of CHROMO domain genes in five monocots, to which both CMT2 and cpSRP43 belong. Results showed that gene copy numbers are similar in monocots to those in Arabidopsis. Phylogenetic analyses split the family into six major clades, among which CMT2 and cpSRP43 formed independent clades, respectively. Two CMT2s are present in the maize genome, while a single cpSRP43 exists in maize. Expression of the CTM2 homologs was elevated 2 and 48 h after heat stress in maize roots, while that of cpSRP43 was increased 2 and 48 h after stress in maize stalks. The genes identified here can be used as molecular targets for breeders to select for thermal-tolerant wheat lines, while phylogenetic and expression analyses of the CHROMO domain genes can be used as a knowledge base for molecular, biochemical and physiological characterization of the genes in monocots.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. D’Hont, A., Denoeud, F., Aury, J.M., Baurens, F.C., Carreel, F., Garsmeur, O., Noel, B., Bocs, S., Droc, G., Rouard, M., Da Silva, C., Jabbari, K., Cardi, C., Poulain, J., Souquet, M., Labadie, K., Jourda, C., Lengelle, J., Rodier-Goud, M., Alberti, A., Bernard, M., Correa, M., Ayyampalayam, S., McKain, M.R., Leebens-Mack, J., Burgess, D., Freeling, M., Mbeguie, A.M.D., Chabannes, M., Wicker, T., Panaud, O., Barbosa, J., Hribova, E., Heslop-Harrison, P., Habas, R., Rivallan, R., Francois, P., Poiron, C., Kilian, A., Burthia, D., Jenny, C., Bakry, F., Brown, S., Guignon, V., Kema, G., Dita, M., Waalwijk, C., Joseph, S., Dievart, A., Jaillon, O., Leclercq, J., Argout, X., Lyons, E., Almeida, A., Jeridi, M., Dolezel, J., Roux, N., Risterucci, A.M., Weissenbach, J., Ruiz, M., Glaszmann, J.C., Quetier, F., Yahiaoui, N., and Wincker, P., The banana (Musa acuminata) genome and the evolution of monocotyledonous plants, Nature, 2012, vol. 488, pp. 213–217. https://doi.org/10.1038/nature11241

    Article  CAS  PubMed  ADS  Google Scholar 

  2. Dubin, M.J., Zhang, P., Meng, D., Remigereau, M.-S., Osborne, E.J., Paolo Casale, F., Drewe, P., Kahles, A., Jean, G., Vilhjálmsson, B., Jagoda, J., Irez, S., Voronin, V., Song, Q., Long, Q., Rätsch, G., Stegle, O., Clark, R.M., and Nordborg, M., DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation, eLife, 2015, vol. 4, p. e05255. https://doi.org/10.7554/eLife.05255

    Article  PubMed  PubMed Central  Google Scholar 

  3. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 2004, vol. 32, pp. 1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Eissenberg, J.C., Molecular biology of the chromo domain: an ancient chromatin module comes of age, Gene, 2001, vol. 275, pp. 19–29. https://doi.org/10.1016/s0378-1119(01)00628-x

    Article  CAS  PubMed  Google Scholar 

  5. Finn, R.D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Heger, A., Hetherington, K., Holm, L., Mistry, J., Sonnhammer, E.L., Tate, J., and Punta, M., Pfam: the protein families database, Nucleic Acids Res, 2014, vol. 42, pp. D222–D230. https://doi.org/10.1093/nar/gkt1223

    Article  CAS  PubMed  Google Scholar 

  6. Finn, R.D., Clements, J., and Eddy, S.R., HMMER web server: interactive sequence similarity searching, Nucleic Acids Res, 2011, vol. 39, pp. W29–W37. https://doi.org/10.1093/nar/gkr367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Gallego-Bartolome, J., DNA methylation in plants: mechanisms and tools for targeted manipulation, New Phytol., 2020, vol. 227, pp. 38–44. https://doi.org/10.1111/nph.16529

    Article  CAS  PubMed  Google Scholar 

  8. Guindon, S., Delsuc, F., Dufayard, J.F., and Gascuel, O., Estimating maximum likelihood phylogenies with PhyML, Methods Mol. Biol., 2009, vol. 537, pp. 113–137. https://doi.org/10.1007/978-1-59745-251-9_6

    Article  CAS  PubMed  Google Scholar 

  9. He, J., Jiang, Z., Gao, L., You, C., Ma, X., Wang, X., Xu, X., Mo, B., Chen, X., and Liu, L., Genome-wide transcript and small RNA profiling reveals transcriptomic responses to heat stress, Plant Physiol., 2019, vol. 181, pp. 609–629. https://doi.org/10.1104/pp.19.00403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Henikoff, S. and Comai, L., A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis, Genetics, 1998, vol. 149, pp. 307–318. https://doi.org/10.1093/genetics/149.1.307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. International Brachypodium I, Genome sequencing and analysis of the model grass Brachypodium distachyon, Nature, 2010, vol. 463, pp. 763–768. https://doi.org/10.1038/nature08747

    Article  CAS  ADS  Google Scholar 

  12. International Rice Genome Sequencing P, The map-based sequence of the rice genome, Nature, 2005, vol. 436, pp. 793–800. https://doi.org/10.1038/nature03895

    Article  CAS  Google Scholar 

  13. Jaru-Ampornpan, P., Liang, F.C., Nisthal, A., Nguyen, T.X., Wang, P., Shen, K., Mayo, S.L., and Shan, S.O., Mechanism of an ATP-independent protein disaggregase: II. Distinct molecular interactions drive multiple steps during aggregate disassembly, J. Biol. Chem., 2013, vol. 288, pp. 13431–13445. https://doi.org/10.1074/jbc.M113.462861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Jaru-Ampornpan, P., Shen, K., Lam, V.Q., Ali, M., Doniach, S., Jia, T.Z., and Shan, S.O., ATP-independent reversal of a membrane protein aggregate by a chloroplast SRP subunit, Nat. Struct. Mol. Biol., 2010, vol. 17, pp. 696–702. https://doi.org/10.1038/nsmb.1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ji, S., Siegel, A., Shan, S.O., Grimm, B., and Wang, P., Chloroplast SRP43 autonomously protects chlorophyll biosynthesis proteins against heat shock, Nat. Plants, 2021, vol. 7, pp. 1420–1432. https://doi.org/10.1038/s41477-021-00994-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jing, Y., Guo, Q., and Lin, R., The chromatin-remodeling factor PICKLE antagonizes Polycomb repression of FT to promote flowering, Plant Physiol., 2019, vol. 181, pp. 656–668. https://doi.org/10.1104/pp.19.00596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kawahara, Y., de la Bastide, M., Hamilton, J.P., Kanamori, H., McCombie, W.R., Ouyang, S., Schwartz, D.C., Tanaka, T., Wu, J., Zhou, S., Childs, K.L., Davidson, R.M., Lin, H., Quesada-Ocampo, L., Vaillancourt, B., Sakai, H., Lee, S.S., Kim, J., Numa, H., Itoh, T., Buell, C.R., and Matsumoto, T., Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data, Rice, 2013, vol. 6, p. 4. https://doi.org/10.1186/1939-8433-6-4

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kumar, S., Suleski, M., Craig, J.M., Kasprowicz, A.E., Sanderford, M., Li, M., Stecher, G., and Hedges, S.B., TimeTree 5: an expanded resource for species divergence times, Mol. Biol. Evol., 2022, vol. 39. https://doi.org/10.1093/molbev/msac174

  19. Li, Z. and Howell, S.H., Heat stress responses and thermotolerance in maize, Int. J. Mol. Sci., 2021, vol. 22. https://doi.org/10.3390/ijms22020948

  20. Li, Z., Tang, J., Srivastava, R., Bassham, D.C., and Howell, S.H., The transcription factor bZIP60 links the unfolded protein response to the heat stress response in maize, Plant Cell, 2020, vol. 32, pp. 3559–3575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Liu, S., de Jonge, J., Trejo-Arellano, M.S., Santos-Gonzalez, J., Kohler, C., and Hennig, L., Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress, New Phytol., 2021, vol. 229, pp. 2238–2250. https://doi.org/10.1111/nph.17018

    Article  CAS  PubMed  Google Scholar 

  22. Liu, Y., Yang, X., Zhou, M., Yang, Y., Li, F., Yan, X., Zhang, M., Wei, Z., Qin, S., and Min, J., Structural basis for the recognition of methylated histone H3 by the Arabidopsis LHP1 chromodomain, J. Biol. Chem., 2022, vol. 298, p. 101623. https://doi.org/10.1016/j.jbc.2022.101623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lizaso, J., Ruiz-Ramos, M., Rodríguez, L., Gabaldon-Leal, C., Oliveira, J., Lorite, I., Sánchez, D., García, E., and Rodríguez, A., Impact of high temperatures in maize: phenology and yield components, Field Crops Res., 2018, vol. 216, pp. 129–140.

    Article  Google Scholar 

  24. Lobell, D.B., Bänziger, M., Magorokosho, C., and Vivek, B., Nonlinear heat effects on African maize as evidenced by historical yield trials, Nat. Climate Change, 2011, vol. 1, pp. 42–45. https://doi.org/10.1038/nclimate1043

    Article  ADS  Google Scholar 

  25. Nguyen, T.X., Jaru-Ampornpan, P., Lam, V.Q., Cao, P., Piszkiewicz, S., Hess, S., and Shan, S.O., Mechanism of an ATP-independent protein disaggregase: I. Structure of a membrane protein aggregate reveals a mechanism of recognition by its chaperone, J. Biol. Chem., 2013, vol. 288, pp. 13420–13430. https://doi.org/10.1074/jbc.M113.462812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Nozawa, K., Masuda, S., Saze, H., Ikeda, Y., Suzuki, T., Takagi, H., Tanaka, K., Ohama, N., Niu, X., Kato, A., and Ito, H., Regulation of ecotype-specific expression of the heat-activated transposon ONSEN, Front. Plant Sci., 2022, vol. 13, p. 899105. https://doi.org/10.3389/fpls.2022.899105

    Article  PubMed  PubMed Central  Google Scholar 

  27. Park, J., Oh, D.H., Dassanayake, M., Nguyen, K.T., Ogas, J., Choi, G., and Sun, T.P., Gibberellin signaling requires chromatin remodeler PICKLE to promote vegetative growth and phase transitions, Plant Physiol., 2017, vol. 173, pp. 1463–1474. https://doi.org/10.1104/pp.16.01471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Reiser, L., Subramaniam, S., Zhang, P., and Berardini, T., Using the Arabidopsis Information Resource (TAIR) to find information about Arabidopsis genes, Curr. Protoc., 2022, vol. 2, p. e574. https://doi.org/10.1002/cpz1.574

    Article  CAS  PubMed  Google Scholar 

  29. Sang, Q., Pajoro, A., Sun, H., Song, B., Yang, X., Stolze, S.C., Andres, F., Schneeberger, K., Nakagami, H., and Coupland, G., Mutagenesis of a quintuple mutant impaired in environmental responses reveals roles for CHROMATIN REMODELING4 in the Arabidopsis floral transition, Plant Cell, 2020, vol. 32, pp. 1479–1500. https://doi.org/10.1105/tpc.19.00992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sasaki, E., Kawakatsu, T., Ecker, J.R., and Nordborg, M., Common alleles of CMT2 and NRPE1 are major determinants of CHH methylation variation in Arabidopsis thaliana, PLoS Genet., 2019, vol. 15, p. e1008492. https://doi.org/10.1371/journal.pgen.1008492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Schuenemann, D., Gupta, S., Persello-Cartieaux, F., Klimyuk, V.I., Jones, J.D., Nussaume, L., and Hoffman, N.E., A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 10312–10316. https://doi.org/10.1073/pnas.95.17.10312

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  32. Shen, X., De Jonge, J., Forsberg, S.K., Pettersson, M.E., Sheng, Z., Hennig, L., and Carlborg, O., Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality, PLoS Genet., 2014, vol. 10, p. e1004842. https://doi.org/10.1371/journal.pgen.1004842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Shen, Y., Devic, M., Lepiniec, L., and Zhou, D.X., Chromodomain, helicase and DNA-binding CHD1 protein, CHR5, are involved in establishing active chromatin state of seed maturation genes, Plant Biotechnol. J., 2015, vol. 13, pp. 811–820. https://doi.org/10.1111/pbi.12315

    Article  CAS  PubMed  Google Scholar 

  34. Van Buren, R., Bryant, D., Edger, P.P., Tang, H., Burgess, D., Challabathula, D., Spittle, K., Hall, R., Gu, J., Lyons, E., Freeling, M., Bartels, D., Ten Hallers, B, Hastie, A., Michael, T.P., and Mockler, T.C., Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum, Nature, 2015 vol. 527, pp. 508–511. https://doi.org/10.1038/nature15714

    Article  CAS  PubMed  ADS  Google Scholar 

  35. Wang, P. and Grimm, B., Comparative analysis of light-harvesting antennae and state transition in chlorina and cpSRP mutants, Plant Physiol., 2016, vol. 172, pp. 1519–1531. https://doi.org/10.1104/pp.16.01009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wang, P., Liang, F.C., Wittmann, D., Siegel, A., Shan, S.O., and Grimm, B., Chloroplast SRP43 acts as a chaperone for glutamyl-tRNA reductase, the rate-limiting enzyme in tetrapyrrole biosynthesis, Proc. Natl. Acad. Sci. U. S. A., 2018, vol. 115, pp. E3588–E3596. https://doi.org/10.1073/pnas.1719645115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yan, B., Lv, Y., Zhao, C., and Wang, X., Knowing when to silence: roles of polycomb-group proteins in SAM maintenance, root development, and developmental phase transition, Int. J. Mol. Sci., 2020, vol. 21. https://doi.org/10.3390/ijms21165871

  38. Yates, A.D., Allen, J., Amode, R.M., Azov, A.G., Barba, M., Becerra, A., Bhai, J., Campbell, L.I., Carbajo Martinez, M., Chakiachvili, M., Chougule, K., Christensen, M., Contreras-Moreira, B., Cuzick, A., Da Rin Fioretto, L., Davis, P., De Silva, N.H., Diamantakis, S., Dyer, S., Elser, J., Filippi, C.V., Gall, A., Grigoriadis, D., Guijarro-Clarke, C., Gupta, P., Hammond-Kosack, K.E., Howe, K.L., Jaiswal, P., Kaikala, V., Kumar, V., Kumari, S., Langridge, N., Le, T., Luypaert, M., Maslen, G.L., Maurel, T., Moore, B., Muffato, M., Mushtaq, A., Naamati, G., Naithani, S., Olson, A., Parker, A., Paulini, M., Pedro, H., Perry, E., Preece, J., Quinton-Tulloch, M., Rodgers, F., Rosello, M., Ruffier, M., Seager, J., Sitnik, V., Szpak, M., Tate, J., Tello-Ruiz, M.K., Trevanion, S.J., Urban, M., Ware, D., Wei, S., Williams, G., Winterbottom, A., Zarowiecki, M., Finn, R.D., and Flicek, P., Ensembl Genomes 2022: an expanding genome resource for non-vertebrates, Nucleic Acids Res., 2022, vol. 50, pp. D996–D1003. https://doi.org/10.1093/nar/gkab1007

    Article  CAS  PubMed  Google Scholar 

  39. Yu, Y., Zhang, H., Long, Y., Shu, Y., and Zhai, J., Plant Public RNA-seq Database: a comprehensive online database for expression analysis of ~45 000 plant public RNA-Seq libraries, Plant Biotechnol. J., 2022, vol. 20, pp. 806–808. https://doi.org/10.1111/pbi.13798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Zhang, H., Lang, Z., and Zhu, J.K., Dynamics and function of DNA methylation in plants, Nat. Rev. Mol. Cell Biol., 2018a, vol. 19, pp. 489–506. https://doi.org/10.1038/s41580-018-0016-z

    Article  CAS  PubMed  Google Scholar 

  41. Zhang, Y., Harris, C.J., Liu, Q., Liu, W., Ausin, I., Long, Y., Xiao, L., Feng, L., Chen, X., Xie, Y., Chen, X., Zhan, L., Feng, S., Li, J.J., Wang, H., Zhai, J., and Jacobsen, S.E., Large-scale comparative epigenomics reveals hierarchical regulation of non-CG methylation in Arabidopsis, Proc. Natl. Acad. Sci. U. S. A., 2018b, vol. 115, pp. E1069–E1074. https://doi.org/10.1073/pnas.1716300115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhang, Y., Wendte, J.M., Ji, L., and Schmitz, R.J., Natural variation in DNA methylation homeostasis and the emergence of epialleles, Proc. Natl. Acad. Sci. U. S. A., 2020, vol. 117, pp. 4874–4884. https://doi.org/10.1073/pnas.1918172117

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  43. Zou, B., Sun, Q., Zhang, W., Ding, Y., Yang, D.L., Shi, Z., and Hua, J., The Arabidopsis chromatin-remodeling factor CHR5 regulates plant immune responses and nucleosome occupancy, Plant Cell Physiol., 2017, vol. 58, pp. 2202–2216. https://doi.org/10.1093/pcp/pcx155

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work is supported by Special Funds for Key Research Development and Promotion of Henan Province (222102110231) and the Key Research and Development Projects of Henan Province (231111113000).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pengfei Duan.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pengfei Duan, Kan, Y., Zhao, D. et al. Genome-Wide Identification and Characterization of CHROMO Domain Family Genes Reveal Roles of the Maize Genes in Heat Stress Response. Biol Bull Russ Acad Sci 50 (Suppl 3), S289–S297 (2023). https://doi.org/10.1134/S1062359022603494

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359022603494

Keywords:

Navigation