Effect of mutations in the Sym7, Sym19 and Sym34 genes on the interaction of pea (Pisum sativum L.) with the arbuscular mycorrhizal fungus Rhizophagus irregularis

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Abstract

BACKGROUND: Within the pea (Pisum sativum L.) species, genotypes with high and low responsiveness to inoculation with arbuscular mycorrhizal fungi can be distinguished.

AIM: The aim of this study was to test the hypothesis that pea responsiveness to arbuscular mycorrhizal fungi inoculation may be inversely correlated with root colonization levels.

MATERIALS AND METHODS: The wild-type line Finale with low responsiveness to arbuscular mycorrhizal fungi inoculation and symbiotic mutants obtained on its basis were used. Plants were grown under controlled climatic conditions with a deficiency of available phosphorus; the fungus Rhizophagus irregularis was used for inoculation. Parameters of plant growth and development of reproductive organs were determined 52 and 71 days after inoculation, which corresponded to the flowering and pod filling stages, respectively.

RESULTS: All mutant lines under conditions without inoculation had generally reduced parameters compared to the original line Finale. Inoculation led to a decrease in many parameters in the line Finale. Mutations in the Sym7 and Sym34 genes, which led to a decrease or delay in the start of mycorrhization, respectively, contributed to the manifestation of a positive plant response to inoculation. The mutant in the Sym19 gene almost completely lacked intrartadical colonization, while inoculation had no effect on the growth and development of above-ground organs.

CONCLUSIONS: The study results support the idea that reducing mycorrhization levels can have a positive effect on pea plants.

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About the authors

Oksana Y. Shtark

All-Russia Research Institute for Agricultural Microbiology

Email: oshtark@yandex.ru
ORCID iD: 0000-0002-3656-4559
SPIN-code: 4934-4465
Scopus Author ID: 21935113900
ResearcherId: J-4063-2018

Cand. Sci. (Biology)

Russian Federation, Saint Petersburg

Aleksandr I. Zhernakov

All-Russia Research Institute for Agricultural Microbiology

Email: azhernakov@gmail.com
ORCID iD: 0000-0001-8961-9317
Russian Federation, Saint Petersburg

Natalia E. Kichigina

All-Russia Research Institute for Agricultural Microbiology

Email: n.kichigina@arriam.ru
ORCID iD: 0000-0002-6568-7988
Russian Federation, Saint Petersburg

Gulnara A. Akhtemova

All-Russia Research Institute for Agricultural Microbiology

Email: ahgulya@yandex.ru
ORCID iD: 0000-0001-7957-3693
SPIN-code: 1714-8554

Cand. Sci. (Biology)

Russian Federation, Saint Petersburg

Anton S. Sulima

All-Russia Research Institute for Agricultural Microbiology

Email: asulima@arriam.ru
ORCID iD: 0000-0002-2300-857X
SPIN-code: 4906-1159

Cand. Sci. (Biology)

Russian Federation, Saint Petersburg

Evgeny A. Zorin

All-Russia Research Institute for Agricultural Microbiology

Email: kjokkjok8@gmail.com
ORCID iD: 0000-0001-5666-3020
SPIN-code: 5048-0203

Cand. Sci. (Biology)

Russian Federation, Saint Petersburg

Vladimir A. Zhukov

All-Russia Research Institute for Agricultural Microbiology

Author for correspondence.
Email: vzhukov@arriam.ru
ORCID iD: 0000-0002-2411-9191
SPIN-code: 2610-3670
Scopus Author ID: 35325957900

Candidate of Biological Sciences, Head of the Laboratory of Genetics of Plant-Microbe Interactions

Russian Federation, Saint Petersburg

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2. Fig. 1. Dynamics of arbuscular mycorrhiza (AM) development in pea plants: Finale (wt) line and RisNod2 (sym19) mutant, inoculated with the fungus Rhizophagus irregularis BEG144. Parameters of AM development: EM% is intensity of external (extraradical) mycelium development; M% is intensity of intraradical mycelium development; a% is abundance of arbuscules in the mycorrhizal part of the root. The values of all three parameters differ significantly (р ≤ 0.05) in the initial line and the mutant at each of the time points. The values of the EM% and M% parameters differ significantly at all three time points in both pea genotypes. Error bars represent the errors of the mean. For the EM% and M% parameters in the mutant, the error bars do not go beyond the data point markers; the values of the a% parameter at 7 DPI in the mutant are equal to “0” in all replicates

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3. Fig. 2. Parameters of root colonization by the arbuscular mycorrhiza fungus Rhizophagus irregularis BEG144 in the Finale pea line and induced mutants with various changes in the development of intraradical and extraradical mycelium at the second analysis stage (stage “filled pod, green seeds”, 71 days after inoculation). M% is the intensity of mycorrhizal colonization; a% is the saturation of mycorrhizal fragments of the root system with arbuscules. *Values for mutants that differ significantly from those for the original line at p ≤ 0.05. Error bars represent the errors of the mean

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4. Fig. 3. Effect of inoculation with the arbuscular mycorrhiza fungus Rhizophagus irregularis BEG144 on the development parameters of the Finale line pea plants and induced mutants with various changes in the development of intraradical and extraradical mycelium at the first stage of analysis (flowering stage, 52 days after inoculation). *Parameter values for the inoculated variant significantly different from the values for the non-inoculated variant of the same pea line at р ≤ 0.05. Error bars represent the errors of the mean. RN is RisNod

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5. Fig. 4. Effect of inoculation with the arbuscular mycorrhiza fungus Rhizophagus irregularis BEG144 on the growth and development parameters of the Finale line pea plants and induced mutants with various changes in the development of the intraradical and extraradical mycelium at the second stage of analysis (stage “filled pod, green seeds”, 71 days after inoculation). *Parameter values for the inoculated variant that are significantly different from the values for the non-inoculated variant of the same pea line at p ≤ 0.05. Error bars represent the errors of the mean. RN is RisNod

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