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Planta

, Volume 248, Issue 5, pp 1101–1120 | Cite as

Role of a receptor-like kinase K1 in pea Rhizobium symbiosis development

  • Anna N. Kirienko
  • Yuri B. Porozov
  • Nikita V. Malkov
  • Gulnara A. Akhtemova
  • Christine Le Signor
  • Richard Thompson
  • Christine Saffray
  • Marion Dalmais
  • Abdelhafid Bendahmane
  • Igor A. Tikhonovich
  • Elena A. Dolgikh
Original Article

Abstract

Main conclusion

The LysM receptor-like kinase K1 is involved in regulation of pea-rhizobial symbiosis development.

The ability of the crop legume Pisum sativum L. to perceive the Nod factor rhizobial signals may depend on several receptors that differ in ligand structure specificity. Identification of pea mutants defective in two types of LysM receptor-like kinases (LysM-RLKs), SYM10 and SYM37, featuring different phenotypic manifestations and impaired at various stages of symbiosis development, corresponds well to this assumption. There is evidence that one of the receptor proteins involved in symbiosis initiation, SYM10, has an inactive kinase domain. This implies the presence of an additional component in the receptor complex, together with SYM10, that remains unknown. Here, we describe a new LysM-RLK, K1, which may serve as an additional component of the receptor complex in pea. To verify the function of K1 in symbiosis, several P. sativum non-nodulating mutants in the k1 gene were identified using the TILLING approach. Phenotyping revealed the blocking of symbiosis development at an appropriately early stage, strongly suggesting the importance of LysM-RLK K1 for symbiosis initiation. Moreover, the analysis of pea mutants with weaker phenotypes provides evidence for the additional role of K1 in infection thread distribution in the cortex and rhizobia penetration. The interaction between K1 and SYM10 was detected using transient leaf expression in Nicotiana benthamiana and in the yeast two-hybrid system. Since the possibility of SYM10/SYM37 complex formation was also shown, we tested whether the SYM37 and K1 receptors are functionally interchangeable using a complementation test. The interaction between K1 and other receptors is discussed.

Keywords

Heterologous expression Legume-Rhizobium symbiosis LysM receptor-like kinases Mutants Nod factor perception Pea Pisum sativum L. 

Abbreviations

ECD

Extracellular domain

GUS

Beta-glucuronidase

HR

Hypersensitivity reaction

IT

Infection thread

RLK

Receptor-like kinase

Y2H

Yeast two-hybrid system

Notes

Acknowledgements

This work was funded for ARRIAM (A.N.K., N.V.M., G.A.A., I.A.T., and E.A.D.) by Russian Scientific Foundation (RSF project no. 16-16-10043) and for ITMO University (Yu.B.P) by Government of Russian Federation, Grant 074-U01. The INRA TILLING activities are supported by the Program Saclay Plant Sciences (SPS, ANR-10-LABX-40) and the European Research Council (ERC-SEXYPARTH). The research was performed using the equipment of the Core Center “Genomic technologies, proteomics and cellular biology” at ARRIAM. We are very grateful to Dr. Julie Cullimore (Laboratory of Plant–Microbe Interactions, INRA, France) for kindly providing the constructs for production of AtCERK1-ECD in yeast and for the pMON and pBIN vectors. Dr. Zhukov V. and Sulima A. for providing K1 and Sym37 sequences (cv. Cameor). Kitaeva A. for helping in microscopy analysis.

Compliance with ethical standards

Conflicts of interest

No conflicts of interest declared.

Supplementary material

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Anna N. Kirienko
    • 1
  • Yuri B. Porozov
    • 2
    • 3
  • Nikita V. Malkov
    • 1
  • Gulnara A. Akhtemova
    • 1
  • Christine Le Signor
    • 4
  • Richard Thompson
    • 4
  • Christine Saffray
    • 5
  • Marion Dalmais
    • 5
  • Abdelhafid Bendahmane
    • 5
  • Igor A. Tikhonovich
    • 1
  • Elena A. Dolgikh
    • 1
  1. 1.All-Russia Research Institute for Agricultural MicrobiologySt. PetersburgRussia
  2. 2.ITMO UniversitySt. PetersburgRussia
  3. 3.I.M. Sechenov First Moscow State Medical UniversityMoscowRussia
  4. 4.Agroécologie, AgroSup Dijon, INRA, Univ. Bourgogne Franche-ComtéDijonFrance
  5. 5.IPS2, UMR9213/UMR1403, CNRS, INRA, UPSud, UPD, SPSOrsayFrance

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