Unique transcriptome features of pea (Pisum sativum L.) lines with differing responses to beneficial soil microorganisms

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Abstract

BACKGROUND: Garden pea (Pisum sativum L.) possesses the ability to form beneficial symbioses with various soil microorganisms. However, different pea cultivars, genotypes, and lines gain more or less benefit from these interactions, so the trait named “efficiency of interaction with soil microorganisms” (EIBSM) was suggested to describe this phenomenon. The molecular mechanisms underlying the manifestation of the EIBSM trait are not properly studied, and only few works focusing on plant responses to combined microbial preparations have been published to date.

METHODS: Eight pea lines previously described as contrasting in manifestation of the EIBSM trait were grown in pots with soil under combined inoculation with nodule bacteria and arbuscular mycorrhizal fungi, and the transcriptome profiles of the whole root systems of the plants were investigated using 3'MACE RNA sequencing.

RESULTS: The relatedness of the lines inferred from the analysis of transcripts’ SNVs (Single Nucleotide Variants) corresponded to the manifestation of the EIBSM trait: three high-EIBSM lines and three low-EIBSM lines formed two distinct clusters. Thus, the gene expression profiles were compared between these two clusters, which enabled identification of transcriptome signatures characteristic for each group. The lines previously described as high-EIBSM have lower symbiotic activity, and the expression levels of pathogen response genes were elevated compared to the lines with low EIBSM.

CONCLUSION: This result suggests that the mechanism of high interaction efficiency may be connected to stricter host control of symbionts, allowing such plants to expend less on the symbioses.

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About the authors

Alexey M. Afonin

All-Russia Research Institute for Agricultural Microbiology

Author for correspondence.
Email: afoninalexeym@gmail.com
ORCID iD: 0000-0002-8530-0226

Research engineer

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Emma S. Gribchenko

All-Russia Research Institute for Agricultural Microbiology

Email: gribemma@gmail.com
ORCID iD: 0000-0002-1538-5527

Technician

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Evgeny A. Zorin

All-Russia Research Institute for Agricultural Microbiology

Email: kjokkjok8@gmail.com
ORCID iD: 0000-0001-5666-3020

Research engineer

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Anton S. Sulima

All-Russia Research Institute for Agricultural Microbiology

Email: asulima@arriam.ru
ORCID iD: 0000-0002-2300-857X

PhD, Cand. Sci. (Biol.)

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Daria A. Romanyuk

All-Russia Research Institute for Agricultural Microbiology

Email: daria-rom@yandex.ru
ORCID iD: 0000-0001-9576-1256

PhD, Cand. Sci. (Biol.)

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Alexander I. Zhernakov

All-Russia Research Institute for Agricultural Microbiology

Email: azhernakov@arriam.ru
ORCID iD: 0000-0001-8961-9317
Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Oksana Yu. Shtark

All-Russia Research Institute for Agricultural Microbiology

Email: oshtark@arriam.ru
ORCID iD: 0000-0002-3656-4559

PhD, Cand. Sci. (Biol.)

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Gulnar A. Akhtemova

All-Russia Research Institute for Agricultural Microbiology

Email: gakhtemova@arriam.ru
ORCID iD: 0000-0001-7957-3693

PhD, Cand. Sci. (Biol.)

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

Vladimir A. Zhukov

All-Russia Research Institute for Agricultural Microbiology

Email: vzhukov@arriam.ru
ORCID iD: 0000-0002-2411-9191

PhD, Cand. Sci. (Biol.)

Russian Federation, 3, Podbelsky highway, Pushkin, Saint Petersburg, 196608

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Supplementary files

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1. Fig. 1. The tree shows the genetic relatedness of pea lines. The distance was calculated using Provesti’s distance algorithm of the poppr [28], the bootstrap values are presented in the nodes of the tree. The high-EIBSM lines are denoted with “*”

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2. Fig. 2. The PCA plot for the six lines with contrast manifestation of the EIBSM trait. The high-EIBSM lines are denoted with “*”, 95% confidence ellipses were built for the two discussed groups

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3. Fig. 3. The functional categories of genes, differing in their expression in EIBSM-contrasting lines. The bars represent the number of genes in the category, the bars to the right are genes with higher expression level in the ‘high-EIBSM’ lines, and vice versa

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