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Arbuscular mycorrhiza development in pea (Pisum sativum L.) mutants impaired in five early nodulation genes including putative orthologs of NSP1 and NSP2

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Abstract

Arbuscular mycorrhiza (AM) development in five non-nodulating pea (Pisum sativum L.) mutants (sym7, sym11, sym14, sym34, sym38) grown in nurse pots was analyzed at the early stages of colonization by Rhizophagus irregularis. Abundance of external mycelium attached to the root surface and parameters of internal fungal colonization, i.e. intensity of colonization, and arbuscule and vesicle/spore abundance, were evaluated. Mutations in SYM7 (putative ortholog of NSP2, ‘nodulation signaling pathway 2’), SYM11, and SYM14 genes resulted in considerable increase in root surface colonization and a substantial decrease in internal colonization as compared to corresponding wild-type pea lines (wt). In addition, the mutants sym7 and sym11 displayed a highly reduced amount of arbuscules. In contrast, plants mutated for the SYM34 gene displayed strongly reduced root surface colonization. The mutant sym34 also had strongly reduced internal colonization after 10 days of growth, but did not differ from wt 10 days later. The sym38 mutant did not differ from wt. These data indicate that all pea genes analyzed, except SYM38, are essential for both nodule and AM development. The phenotype of sym34 suggested that the pea SYM34 gene is an ortholog of the Medicago truncatula NSP1 (‘nodulation signaling pathway 1’), and early stop codons were in fact detected in an NSP1 homologous sequence of two sym34 mutants. In addition, full co-segregation of the allelic states of a molecular marker representing a polymorphic fragment of the hypothetical pea NSP1 gene, together with the nodulation phenotype of 50 F2 plants, support our hypothesis. A possible explanation for the different AM phenotypes of sym7 and sym34 is given.

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Abbreviations

AM:

Arbuscular mycorrhiza(l)

CM(s):

Cutin monomer(s)

CSSP:

Common symbiotic signaling pathway

IT:

Infection thread

PPA:

Pre-penetration apparatus

RN:

Root nodules

SL(s):

Strigolactone(s)

TF(s):

Transcription factor(s)

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Acknowledgments

We appreciate the help of Dr. Frédérique C. Guinel (Biology Department, Wilfrid Laurier University, Waterloo, Canada) and Dr. Vivienne Gianinazzi-Pearson for English improvement and critical reading of the manuscript, and that of Ms. Eugenia A. Shtark for her assistance in preparing the illustrations. We thank Lyudmila E. Dvoryaninova, Darya M. Shulgina, and Darya A. Khodareva (ARRIAM, Saint-Petersburg, Russia) for their excellent technical assistance. The research was performed using equipment of the Core Center ‘Genomic Technologies, Proteomics and Cell Biology’ in ARRIAM. The part of the work represented in Sections 3.1, 4.1, and 4.3 was supported by Grants of the President of the Russian Federation for leading Russian scientific school (4603.2014.4) and Russian Foundation for Basic Research (RFBR) (13-04-01702; 13-04-01703; 15-29-02737). The part of the work represented in Sections 3.2, and 4.2 was supported by a grant of Russian Scientific Foundation (14-24-00135).

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  1. All-Russia Research Institute for Agricultural Microbiology (ARRIAM), Podbelsky chaussee 3, 196608, Pushkin, Saint-Petersburg, Russia

    Oksana Y. Shtark, Anton S. Sulima, Alexander I. Zhernakov, Marina S. Kliukova, Jaroslava V. Fedorina, Alexander G. Pinaev, Alexey A. Kryukov, Gulnara A. Akhtemova, Igor A. Tikhonovich & Vladimir A. Zhukov

  2. Faculty of Biology, Saint-Petersburg State University, Universitetskaya nab. 7/9, 199034, Saint-Petersburg, Russia

    Marina S. Kliukova & Igor A. Tikhonovich

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  1. Oksana Y. Shtark
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  2. Anton S. Sulima
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  3. Alexander I. Zhernakov
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Correspondence to Oksana Y. Shtark.

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Shtark, O.Y., Sulima, A.S., Zhernakov, A.I. et al. Arbuscular mycorrhiza development in pea (Pisum sativum L.) mutants impaired in five early nodulation genes including putative orthologs of NSP1 and NSP2 . Symbiosis 68, 129–144 (2016). https://doi.org/10.1007/s13199-016-0382-2

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