Skip to main content

Advertisement

SpringerLink
Log in

The Rpf84 gene, encoding a ribosomal large subunit protein, RPL22, regulates symbiotic nodulation in Robinia pseudoacacia

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

A homologue of the ribosomal protein L22e, Rpf84, regulates root nodule symbiosis by mediating the infection process of rhizobia and preventing bacteroids from degradation in Robinia pseudoacacia.

Abstract

Ribosomal proteins (RPs) are known to have extraribosomal functions, including developmental regulation and stress responses; however, the effects of RPs on symbiotic nodulation of legumes are still unclear. Ribosomal protein 22 of the large 60S subunit (RPL22), a non-typical RP that is only found in eukaryotes, has been shown to function as a tumour suppressor in animals. Here, a homologue of RPL22, Rpf84, was identified from the leguminous tree R. pseudoacacia. Subcellular localization assays showed that Rpf84 was expressed in the cytoplasm and nucleus. Knockdown of Rpf84 by RNA interference (RNAi) technology impaired the infection process and nodule development. Compared with the control, root and stem length, dry weight and nodule number per plant were drastically decreased in Rpf84-RNAi plants. The numbers of root hair curlings, infection threads and nodule primordia were also significantly reduced. Ultrastructure analyses showed that Rpf84-RNAi nodules contained fewer infected cells with fewer bacteria. In particular, remarkable deformation of bacteroids and fusion of multiple symbiosomes occurred in infected cells. By contrast, overexpression of Rpf84 promoted nodulation, and the overexpression nodules maintained a larger infection/differentiation region and had more infected cells filled with bacteroids than the control at 45 days post inoculation, suggesting a retarded ageing process in nodules. These results indicate for the first time that RP regulates the symbiotic nodulation of legumes and that RPL22 may function in initiating the invasion of rhizobia and preventing bacteroids from degradation in R. pseudoacacia.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

Dpi:

Days post-inoculation

GFP:

Green fluorescent protein

GUS:

β-Glucuronidase

IT:

Infection thread

Lb:

Leghaemoglobin

RNAi:

RNA interference

RP:

Ribosomal protein

RPL:

Ribosomal large subunit protein

TEM:

Transmission electron microscopy

References

  • Antolin-Llovera M, Petutsching EK, Ried MK, Lipka V, Nurnberger T, Robatzek S, Parniske M (2014) Knowing your friends and foes–plant receptor-like kinases as initiators of symbiosis or defence. New Phytol 204:791–802

    Article  CAS  PubMed  Google Scholar 

  • Barakat A, Szick-Miranda K, Chang IF, Guyot R, Blanc G, Cooke R, Delseny M, Bailey-Serres J (2001) The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol 127:398–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N, Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol Plant Microbe Interact 13:1170–1176

    Article  CAS  PubMed  Google Scholar 

  • Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14:695–700

    Article  CAS  PubMed  Google Scholar 

  • Breakspear A, Liu CW, Roy S et al (2014) The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26:4680–4701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrne ME (2009) A role for the ribosome in development. Trends Plant Sci 14:512–519

    Article  CAS  PubMed  Google Scholar 

  • Carroll AJ, Heazlewood JL, Ito J, Millar AH (2008) Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol Cell Proteom 7:347–369

    Article  CAS  Google Scholar 

  • Carvalho CM, Santos AA, Pires SR, Rocha CS, Saraiva DI, Machado JPB, Mattos EC, Fietto LG, Fontes EPB (2008) Regulated nuclear trafficking of rpL10A mediated by NIK1 represents a defense strategy of plant cells against virus. PLoS Pathog 4:e1000247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Casati P, Walbot V (2003) Gene expression profiling in response to ultraviolet radiation in maize genotypes with varying flavonoid content. Plant Physiol 132:1739–1754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang IF, Szick-Miranda K, Pan SQ, Bailey-Serres J (2005) Proteomic characterization of evolutionarily conserved and variable proteins of arabidopsis cytosolic ribosomes. Plant Physiol 137:848–862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen HY, Chou MX, Wang XY, Liu SS, Zhang FL, Wei GH (2013) Profiling of differentially expressed genes in roots of Robinia pseudoacacia during nodule development using suppressive subtractive hybridization. PLoS One 8:e63930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi YL, Tsukasaki K, O’Neill MC et al (2007) A genomic analysis of adult T-cell leukemia. Oncogene 26:1245–1255

    Article  CAS  PubMed  Google Scholar 

  • Dobbelstein M, Shenk T (1995) In vitro selection of RNA ligands for the ribosomal L22 protein associated with Epstein–Barr virus-expressed RNA by using randomized and cDNA-derived RNA libraries. J Virol 69:8027–8034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fahl SP, Wang MS, Zhang Y, Duc ACE, Wiest DL (2015) Regulatory roles of rpl22 in hematopoiesis: an old dog with new tricks. Crit Rev Immunol 35:379–400

    Article  PubMed  PubMed Central  Google Scholar 

  • Fåhraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16:374–381

    PubMed  Google Scholar 

  • Falcone Ferreyra ML, Pezza A, Biarc J, Burlingame AL, Casati P (2010) Plant L10 ribosomal proteins have different roles during development and translation under ultraviolet-B stress. Plant Physiol 153:1878–1894

    Article  CAS  PubMed  Google Scholar 

  • Falcone Ferreyra ML, Casadevall R, Luciani MD, Pezza A, Casati P (2013) New evidence for differential roles of L10 ribosomal proteins from Arabidopsis. Plant Physiol 163:378–391

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fournier J, Teillet A, Chabaud M, Ivanov S, Genre A, Limpens E, de Carvalho-Niebel F, Barker DG (2015) Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiol 167:1233–1242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89–102

    Article  CAS  PubMed  Google Scholar 

  • Horiguchi G, Molla-Morales A, Perez-Perez JM, Kojima K, Robles P, Ponce MR, Micol JL, Tsukaya H (2011) Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J 65:724–736

    Article  CAS  PubMed  Google Scholar 

  • Houmani JL, Davis CI, Ruf IK (2009) Growth-promoting properties of Epstein–Barr virus EBER-1 RNA correlate with ribosomal protein L22 binding. J Virol 83:9844–9853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse MG, Ireland JA, Prem SM, Chen AS, Ware VC (2013) RpL22e, but not RpL22e-like-PA, is SUMOylated and localizes to the nucleoplasm of Drosophila meiotic spermatocytes. Nucleus 4:241–258

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim SJ, Strich R (2016) Rpl22 is required for IME1 mRNA translation and meiotic induction in S. cerevisiae. Cell Div 11:10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim KY, Park SW, Chung YS, Chung CH, Kim JI, Lee JH (2004) Molecular cloning of low-temperature-inducible ribosomal proteins from soybean. J Exp Bot 55:1153–1155

    Article  CAS  PubMed  Google Scholar 

  • Le SY, Sternglanz R, Greider CW (2000) Identification of two RNA-binding proteins associated with human telomerase RNA. Mol Biol Cell 11:999–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Moin M, Bakshi A, Madhav MS, Kirti PB (2017) Expression profiling of ribosomal protein gene family in dehydration stress responses and characterization of transgenic rice plants overexpressing RPL23A for water-use efficiency and tolerance to drought and salt stresses. Front Chem 5:97

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nagaraj S, Senthil-Kumar M, Ramu VS, Wang KR, Mysore KS (2016) Plant ribosomal proteins, RPL12 and RPL19, play a role in nonhost disease resistance against bacterial pathogens. Front Plant Sci 6:1192

    Article  PubMed  PubMed Central  Google Scholar 

  • Ni JQ, Liu LP, Hess D, Rietdorf J, Sun FL (2006) Drosophila ribosomal proteins are associated with linker histone H1 and suppress gene transcription. Genes Dev 20:1959–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429

    Article  CAS  PubMed  Google Scholar 

  • Nishimura T, Wada T, Yamamoto KT, Okada K (2005) The Arabidopsis STV1 protein, responsible for translation reinitiation, is required for auxin-mediated gynoecium patterning. Plant Cell 17:2940–2953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263

    Article  CAS  PubMed  Google Scholar 

  • O’Leary MN, Schreiber KH, Zhang Y et al (2013) The ribosomal protein Rpl22 controls ribosome composition by directly repressing expression of its own paralog, Rpl22l1. PLoS Genet 9:e1003708

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J et al (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  CAS  PubMed  Google Scholar 

  • Rao SY, Lee SY, Gutierrez A et al (2012) Inactivation of ribosomal protein L22 promotes transformation by induction of the stemness factor, Lin28B. Blood 120:3764–3773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosado A, Li RX, van de Ven W, Hsu E, Raikhel NV (2012) Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors. Proc Natl Acad Sci USA 109:19537–19544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roux B, Rodde N, Jardinaud MF et al (2014) An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J 77:817–837

    Article  CAS  PubMed  Google Scholar 

  • Roy S, Robson F, Lilley J et al (2017) MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis. Plant Physiol 174:326–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutkowski R, Hofmann K, Gartner A (2010) Phylogeny and function of the invertebrate p53 superfamily. Cold Spring Harb Perspect Biol 2:a001131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Savada RP, Bonham-Smith PC (2014) Differential transcript accumulation and subcellular localization of Arabidopsis ribosomal proteins. Plant Sci 223:134–145

    Article  CAS  PubMed  Google Scholar 

  • Solanki NR, Stadanlick JE, Zhang Y, Duc AC, Lee SY, Lauritsen JPH, Zhang ZQ, Wiest DL (2016) Rp122 loss selectively impairs αβ T cell development by dysregulating endoplasmic reticulum stress signaling. J Immunol 197:2280–2289

    Article  CAS  PubMed  Google Scholar 

  • Sormani R, Masclaux-Daubresse C, Daniele-Vedele F, Chardon F (2011) Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana. PLoS One 6:e28070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soyano T, Hirakawa H, Sato S, Hayashi M, Kawaguchi M (2014) NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. Proc Natl Acad Sci USA 111:14607–14612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steffen KK, MacKay VL, Kerr EO et al (2008) Yeast life span extension by depletion of 60S ribosomal subunits is mediated by Gcn4. Cell 133:292–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steffen KK, McCormick MA, Pham KM, MacKay VL, Delaney JR, Murakami CJ, Kaeberlein M, Kennedy BK (2012) Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae. Genetics 191:107–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139:3997–4006

    Article  CAS  PubMed  Google Scholar 

  • Szakonyi D, Byrne ME (2011) Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J 65:269–281

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toczyski DP, Matera AG, Ward DC, Steitz JA (1994) The Epstein–Barr-Virus (EBV) small RNA EBER1 binds and relocalizes ribosomal rrotein L22 in EBV-infected human B-lymphocytes. Proc Natl Acad Sci USA 91:3463–3467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasse J, De Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voisin AS, Salon C, Jeudy C, Warembourg FR (2003) Symbiotic N2 fixation activity in relation to C economy of Pisum sativum L. as a function of plant phenology. J Exp Bot 54(393):2733–2744

    Article  CAS  PubMed  Google Scholar 

  • Wei GH, Chen WM, Zhu WF, Chen C, Young JPW, Bontemps C (2009) Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiol Ecol 68:320–328

    Article  CAS  PubMed  Google Scholar 

  • Xiao TT, Schilderink S, Moling S, Deinum EE, Kondorosi E, Franssen H, Kulikova O, Niebel A, Bisseling T (2014) Fate map of Medicago truncatula root nodules. Development 141:3517–3528

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Sun H, He J, Wang H, Yu X, Ma L, Zhu C (2014) Interaction of ribosomal protein L22 with casein kinase 2alpha: a novel mechanism for understanding the biology of non-small cell lung cancer. Oncol Rep 32:139–144

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Duc AC, Rao S, Sun XL, Bilbee AN, Rhodes M, Li Q, Kappes DJ, Rhodes J, Wiest DL (2013) Control of hematopoietic stem cell emergence by antagonistic functions of ribosomal protein paralogs. Dev Cell 24:411–425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, O’Leary MN, Peri S et al (2017) Ribosomal proteins Rpl22 and Rpl22l1 control morphogenesis by regulating pre-mRNA splicing. Cell Rep 18:545–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng M, Wang YH, Liu X et al (2016) The RICE MINUTE-LIKE1 (RML1) gene, encoding a ribosomal large subunit protein L3B, regulates leaf morphology and plant architecture in rice. J Exp Bot 67:3457–3469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou F, Roy B, von Arnim AG (2010) Translation reinitiation and development are compromised in similar ways by mutations in translation initiation factor eIF3 h and the ribosomal protein RPL24. BMC Plant Biol 10:193

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou X, Liao WJ, Liao JM, Liao P, Lu H (2015) Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol 7:92–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Key Research and Development Program of China (Grant no. 2016YFD0800706), the National Natural Science Foundation of China (Grant no. 31172252) and the Shaanxi Province Natural Science Foundation of China (Grant no. 2016JM3004).

Author information

Author notes

  1. Zhao Feng

    Present address: College of Medical Technology, Shaanxi University of Chinese Medicine, Xianyang, 712046, China

  2. Zhao Feng and Lu Zhang contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Yangling, 712100, China

    Zhao Feng, Lu Zhang, Yuanyuan Wu, Li Wang, Mingying Xu, Mo Yang, Yajuan Li, Gehong Wei & Minxia Chou

Authors
  1. Zhao Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuanyuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mingying Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mo Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yajuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gehong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Minxia Chou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Minxia Chou.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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.

Supplementary material 1 (PDF 181 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feng, Z., Zhang, L., Wu, Y. et al. The Rpf84 gene, encoding a ribosomal large subunit protein, RPL22, regulates symbiotic nodulation in Robinia pseudoacacia. Planta 250, 1897–1910 (2019). https://doi.org/10.1007/s00425-019-03267-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03267-3

Keywords

Search

Navigation