SpringerLink
Log in

Identification and expression characteristics of NLP (NIN-like protein) gene family in pepper (Capsicum annuum L.)

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

Pepper (Capsicum annum L.) is the main crop in the vegetable industry. The growth and development of peppers are regulated by nitrate, but there is limited research on the molecular mechanisms of nitrate absorption and assimilation in peppers. A plant specific transcription factor NLP plays an important role in nitrate signal transduction.

Methods and results

In this study, a total of 7 NLP members were identified based on pepper genome data. Two nitrogen transport elements (GCN4) were found in the CaNLP5 promoter. In the phylogenetic tree, CaNLP members are divided into three branches, with pepper NLP and tomato NLP having the closest genetic relationship. The expression levels of CaNLP1, CaNLP3, and CaNLP4 are relatively high in the roots, stems, and leaves. The expression level of CaNLP7 gene is relatively high during the 5–7 days of pepper fruit color transformation. After various non-Biotic stress and hormone treatments, the expression of CaNLP1 was at a high level. The expression of CaNLP3 and CaNLP4 was down regulated in leaves, but up regulated in roots. Under conditions of nitrogen deficiency and sufficient nitrate, the expression patterns of NLP genes in pepper leaves and roots were determined.

Conclusion

These results provide important insights into the multiple functions of CaNLPs in regulating nitrate absorption and transport.

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

Access this article

Log in via an institution

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

All data are available when need.

References

  1. Bloom AJ (2015) The increasing importance of distinguishing among plant nitrogen sources. Curr Opin Plant Biol 25:10–16. https://doi.org/10.1016/j.pbi.2015.03.002

    Article  CAS  PubMed  Google Scholar 

  2. Fredes I, Moreno S, Díaz FP, Gutiérrez RA (2019) Nitrate signaling and the control of Arabidopsis growth and development. Curr Opin Plant Biol 47:112–118. https://doi.org/10.1016/j.pbi.2018.10.004

    Article  CAS  PubMed  Google Scholar 

  3. Ohyama T. (2010). Nitrogen as a major essential element of plants (Vol. 37): Research Signpost

  4. Tegeder M, Masclaux Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217(1):35–53. https://doi.org/10.1111/nph.14876

    Article  PubMed  Google Scholar 

  5. Baenas N, Belović M, Ilic N, Moreno DA, García-Viguera C (2019) Industrial use of pepper (Capsicum annum L.) derived products: technological benefits and biological advantages. Food Chem 274:872–885. https://doi.org/10.1016/j.foodchem.2018.09.047

    Article  CAS  PubMed  Google Scholar 

  6. Jarret RL, Barboza GE, Da Costa Batista FR, Berke T, Chou Y, Hulse-Kemp A et al (2019) Capsicum-an abbreviated compendium. J Am Soc Hortic Sci 144(1):3–22. https://doi.org/10.21273/JASHS04446-18

    Article  Google Scholar 

  7. Schauser L, Handberg K, Sandal N, Stiller J, Thykjær T, Pajuelo E et al (1998) Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol General Genet MGG 259(4):414–423. https://doi.org/10.1007/s004380050831

    Article  CAS  Google Scholar 

  8. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402(6758):191–195. https://doi.org/10.1038/46058

    Article  CAS  PubMed  Google Scholar 

  9. Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and lotus japonicus. J Mol Evol 60(2):229–237. https://doi.org/10.1007/s00239-004-0144-2

    Article  CAS  PubMed  Google Scholar 

  10. Chardin C, Girin T, Roudier F, Meyer C, Krapp A (2014) The plant RWP-RK transcription factors: key regulators of nitrogen responses and of gametophyte development. J Exp Bot 65(19):5577–5587. https://doi.org/10.1093/jxb/eru261

    Article  CAS  PubMed  Google Scholar 

  11. Hsin K, Yang T, Lee Y, Cheng Y (2021) Phylogenetic and structural analysis of NIN-like proteins with a type I/II PB1 domain that regulates oligomerization for nitrate response. Front Plant Sci 12:672035. https://doi.org/10.3389/fpls.2021.672035

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sumimoto H, Kamakura S (2007) Ito T (2007) Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci STKE 401:e6. https://doi.org/10.1126/stke.4012007re6

    Article  Google Scholar 

  13. Ge M, Liu Y, Jiang L, Wang Y, Lv Y, Zhou L et al (2018) Genome-wide analysis of maize NLP transcription factor family revealed the roles in nitrogen response. Plant Growth Regul 84(1):95–105. https://doi.org/10.1007/s10725-017-0324-x

    Article  CAS  Google Scholar 

  14. Lin Z, Guo C, Lou S, ** S, Zeng W, Guo Y et al (2021) Functional analyses unveil the involvement of moso bamboo (Phyllostachys edulis) group I and II NIN-LIKE PROTEINS in nitrate signaling regulation. Plant Sci 306:110862. https://doi.org/10.1016/j.plantsci.2021.110862

    Article  CAS  PubMed  Google Scholar 

  15. Liu M, Zhi X, Wang Y, Wang Y (2021) Genome-wide survey and expression analysis of NIN-like Protein (NLP) genes reveals its potential roles in the response to nitrate signaling in tomato. Bmc Plant Biol 21(1):1–12. https://doi.org/10.1186/s12870-021-03116-0

    Article  CAS  Google Scholar 

  16. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet Mercey S et al (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57(3):426–435. https://doi.org/10.1111/j.1365-313X.2008.03695.x

    Article  CAS  PubMed  Google Scholar 

  17. Yu L, Wu J, Tang H, Yuan Y, Wang S, Wang Y et al (2016) Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and-sufficient conditions by enhancing nitrogen and carbon assimilation. Sci Rep-Uk 6(1):1–13. https://doi.org/10.1038/srep27795

    Article  CAS  Google Scholar 

  18. Konishi M, Okitsu T, Yanagisawa S (2021) Nitrate-responsive NIN-like protein transcription factors perform unique and redundant roles in Arabidopsis. J Exp Bot 72(15):5735–5750. https://doi.org/10.1093/jxb/erab246

    Article  CAS  PubMed  Google Scholar 

  19. Liu F, Xu Y, Chang K, Li S, Liu Z, Qi S et al (2019) The long noncoding RNA T5120 regulates nitrate response and assimilation in Arabidopsis. New Phytol 224(1):117–131. https://doi.org/10.1111/nph.16038

    Article  CAS  PubMed  Google Scholar 

  20. Yan D, Easwaran V, Chau V, Okamoto M, Ierullo M, Kimura M et al (2016) NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis. Nat Commun 7(1):1–11. https://doi.org/10.1038/ncomms13179

    Article  CAS  Google Scholar 

  21. Cao H, Qi S, Sun M, Li Z, Yang Y, Crawford NM et al (2017) Overexpression of the maize ZmNLP6 and ZmNLP8 can complement the Arabidopsis nitrate regulatory mutant nlp7 by restoring nitrate signaling and assimilation. Front Plant Sci 8:1703. https://doi.org/10.3389/fpls.2017.01703

    Article  PubMed  PubMed Central  Google Scholar 

  22. Luo Z, Moreau C, Wang J, Frugier F, **e F (2022) NLP1 binds the CEP1 signalling peptide promoter to repress its expression in response to nitrate. New Phytol 234(5):1547–1552. https://doi.org/10.1111/nph.18062

    Article  CAS  PubMed  Google Scholar 

  23. Liu K, Niu Y, Konishi M, Wu Y, Du H, Sun Chung H et al (2017) Discovery of nitrate-CPK-NLP signalling in central nutrient–growth networks. Nature 545(7654):311–316. https://doi.org/10.1038/nature22077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009

    Article  CAS  PubMed  Google Scholar 

  25. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer EL et al (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49(D1):D412–D419. https://doi.org/10.1093/nar/gkaa913

    Article  CAS  PubMed  Google Scholar 

  26. Duvaud S, Gabella C, Lisacek F, Stockinger H, Ioannidis V, Durinx C (2021) Expasy, the Swiss bioinformatics resource portal, as designed by its users. Nucleic Acids Res 49(W1):W216–W227. https://doi.org/10.1093/nar/gkab225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mu X, Luo J (2019) Evolutionary analyses of NIN-like proteins in plants and their roles in nitrate signaling. Cell Mol Life Sci 76(19):3753–3764. https://doi.org/10.1007/s00018-019-03164-8

    Article  CAS  PubMed  Google Scholar 

  28. Zhao J. (2012). Screening of Reference Genes and Inentification of NBS-LRR Gene Analogs in Pepper (Capsicum Annuum L.)., Nan**g Agricultural University.

  29. Gonzalez DH (2016) Introduction to transcription factor structure and function. In: Gonzalez DH (ed) Plant transcription factors. Elsevier

    Google Scholar 

  30. Kang W, Kim S, Lee H, Choi D, Yeom S (2016) Genome-wide analysis of Dof transcription factors reveals functional characteristics during development and response to biotic stresses in pepper. Sci Rep-Uk 6(1):1–12. https://doi.org/10.1038/srep33332

    Article  CAS  Google Scholar 

  31. Gai W, Ma X, Qiao Y, Shi B, Ul Haq S, Li Q et al (2020) Characterization of the bZIP transcription factor family in pepper (Capsicum annuum L.): CabZIP25 positively modulates the salt tolerance. Front Plant Sci 11:139. https://doi.org/10.3389/fpls.2020.00139

    Article  PubMed  PubMed Central  Google Scholar 

  32. Arce-Rodríguez ML, Martínez O, Ochoa-Alejo N (2021) Genome-wide identification and analysis of the MYB transcription factor gene family in chili pepper (Capsicum spp.). Int J Mol Sci 22(5):2229. https://doi.org/10.3390/ijms22052229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhu MX, Zhang YR, Yang YS, Yang XL, Wang CY, Deng Y et al (2021) Identification and expression analysis of NLP transcription factor family of Chenopodium quinoa Willd. Acta Agriculturae Boreali-Sinica 36(04):37–46. https://doi.org/10.7668/hbnxb.20191913

    Article  Google Scholar 

  34. Wang X, Chen XX, Li HL, Zhang FJ, Zhao XY, Han YP et al (2019) Genome-wide identification and expression pattern analysis of NLP (nin-like protein) transcription factor gene family in apple. Scientia Agricultura Sinica 52(23):4333–4349. https://doi.org/10.3864/j.issn.0578-1752.2019.23.014

    Article  Google Scholar 

  35. Büyük İ, Aybüke O, Aksoy T, Sumer A (2021) The NIN-LIKE PROTEIN (NLP) family in common bean: genome-wide identification, evolution and expression analysis. Commun Faculty Sci Univ Ankara Ser C Biol 30(1):58–84

    Article  Google Scholar 

  36. Liu M, Chang W, Fan Y, Sun W, Qu C, Zhang K et al (2018) Genome-wide identification and characterization of NODULE-INCEPTION-like protein (NLP) family genes in Brassica napus. Int J Mol Sci 19(8):2270. https://doi.org/10.3390/ijms19082270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yuan TT, Zhu CL, Li ZY, Song XZ, Gao ZM (2021) Identification of NLP transcription factors of Phyllostachys edulis and their expression patterns in response to nitrogen. Forest Res 34(05):39–48. https://doi.org/10.13275/j.cnki.lykxyj.2021.005.005

    Article  Google Scholar 

  38. Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E, Colot V et al (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4(1):1–9. https://doi.org/10.1038/ncomms2650

    Article  CAS  Google Scholar 

  39. Magwanga RO, Kirungu JN, Lu P, Cai X, Zhou Z, Xu Y et al (2019) Map-based functional analysis of the GhNLP genes reveals their roles in enhancing tolerance to N-deficiency in cotton. Int J Mol Sci 20(19):4953. https://doi.org/10.3390/ijms20194953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wu XY, Xu ZR, Qu CP, Li W, Sun Q, Liu GJ (2014) Genome-wide identification and characterization of NLP gene family in Populus trichocarpa. Bull Bot Res 34(01):37–43. https://doi.org/10.7525/j.issn.1673-5102.2014.01.006

    Article  CAS  Google Scholar 

  41. Soyano T, Shimoda Y, Hayashi M (2015) Nodule inception antagonistically regulates gene expression with nitrate in Lotus japonicus. Plant Cell Physiol 56(2):368–376. https://doi.org/10.1093/pcp/pcu168

    Article  CAS  PubMed  Google Scholar 

  42. Konishi M, Yanagisawa S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat Commun 4(1):1–9. https://doi.org/10.1038/ncomms2621

    Article  CAS  Google Scholar 

  43. Camargo A, Llamas Á, Schnell RA, Higuera JJ, González-Ballester D, Lefebvre PA et al (2007) Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. Plant Cell 19(11):3491–3503. https://doi.org/10.1105/tpc.106.045922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kumar A, Batra R, Gahlaut V, Gautam T, Kumar S, Sharma M et al (2018) Genome-wide identification and characterization of gene family for RWP-RK transcription factors in wheat (Triticum aestivum L.). PLoS ONE 13(12):e208409. https://doi.org/10.1371/journal.pone.0208409

    Article  CAS  Google Scholar 

  45. Rhaman MS, Imran S, Rauf F, Khatun M, Baskin CC, Murata Y et al (2020) Seed priming with phytohormones: an effective approach for the mitigation of abiotic stress. Plants 10(1):37. https://doi.org/10.3390/plants10010037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Vishal B, Kumar PP (2018) Regulation of seed germination and abiotic stresses by gibberellins and abscisic acid. Front Plant Sci 9:838. https://doi.org/10.3389/fpls.2018.00838

    Article  PubMed  PubMed Central  Google Scholar 

  47. Liu T, Ren T, White PJ, Cong R, Lu J (2018) Storage nitrogen co-ordinates leaf expansion and photosynthetic capacity in winter oilseed rape. J Exp Bot 69(12):2995–3007. https://doi.org/10.1093/jxb/ery134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cao XJ, Lu XP, **ong J, Li J, Wu Q, Zhou FF et al (2016) Cloning and expression of Poncirus Trifoliata (L.) Raf. NIN- like transcription factors under different water conditions. Scientia Agricultura Sinica 49(2):381–390. https://doi.org/10.3864/j.issn.0578-1752.2016.02.018

    Article  CAS  Google Scholar 

  49. **e S, Cao S, Liu Q, **ong X, Lu X (2013) Effect of water deficit stress on isotope 15N uptake and nitrogen metabolism of newhall orange and Yamasitaka Mandarin seedling. J Life Sci 7(11):1170

    CAS  Google Scholar 

Download references

Acknowledgements

I wish to thank Wei Li for advice on experimental design.

Funding

This study was supported by the following projects: genetic diversity analysis and core germplasm construction of pod pepper germplasm resources in southwest China (Project Approval No. 31760576); Integrated application and demonstration of modern and efficient production technologies of pepper in flat farmland above 500 mu area in Yanhe (Qian Ke He Chengguo [2020] No. 1Z005); Research and demonstration of key technology for standardization planting and optimization selection of special raw materials of sour soup (Qian Ke He Zhicheng [2022] Key No. 010); Platform construction project of Engineering Research Center for Protected Vegetable Crops in Higher Learning Institutions of Guizhou Province (Qian Jiao Ji [2022] No. 040); Advantageous industrial cluster construction project of Guizhou pod pepper supported by Ministry of Agriculture and Rural Affairs/Department of Agriculture and Rural Affairs of Guizhou Province (Nong Can Fa [2020] No. 2/Qian Nong Fa [2020] No. 67).

Author information

Authors and Affiliations

  1. College of Agriculture, Guizhou University, Guiyang, 550025, China

    Yuan Wu, Shi-xian Su, Tao Wang, Cha Long & Wei Li

  2. Industry Technology Research Academy of Pepper, Guizhou University, Guiyang, 550025, China

    Yuan Wu, Tao Wang & Wei Li

  3. Research Institute of Pepper, Zunyi, 563000, Guizhou Province, China

    Gui-Hua Peng & Lei He

  4. Engineering Research Center for Protected Vegetable Crops in Higher Learning Institutions of Guizhou Province, Guiyang, 550025, China

    Yuan Wu, Shi-xian Su, Cha Long & Wei Li

Authors
  1. Yuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shi-xian Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gui-Hua Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lei He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cha Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

WY designed the experiment and wrote the article. SSX and WT analysed the data. PGH and HL performed experiments. LC has made optimizations to the charts. LW helped write this article.

Corresponding author

Correspondence to Wei Li.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Ethical approval

This article contains no studies involving humans or animals performed by any of the authors.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Y., Su, Sx., Wang, T. et al. Identification and expression characteristics of NLP (NIN-like protein) gene family in pepper (Capsicum annuum L.). Mol Biol Rep 50, 6655–6668 (2023). https://doi.org/10.1007/s11033-023-08587-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-023-08587-y

Keywords

Search

Navigation