Unique transcriptome features of pea (Pisum sativum L.) lines with differing responses to beneficial soil microorganisms
Alexey M. Afonin , Emma S. Gribchenko , Evgeny A. Zorin , Anton S. Sulima , Daria A. Romanyuk , Alexander I. Zhernakov , Oksana Yu. Shtark , Gulnar A. Akhtemova , Vladimir A. Zhukov
Ecological Genetics ›› 2021, Vol. 19 ›› Issue (2) : 131 -141.
Unique transcriptome features of pea (Pisum sativum L.) lines with differing responses to beneficial soil microorganisms
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.
transcriptomics / Pisum sativum L. / nodule bacteria / arbuscular mycorrhiza / effectiveness of symbiosis
| [1] |
Tsyganov VE, Tsyganova AV. Symbiotic Regulatory Genes Controlling Nodule Development in Pisum sativum L. Plants. 2020;9(12):1741. DOI: 10.3390/plants9121741 |
| [2] |
Tsyganov V.E., Tsyganova A.V. Symbiotic Regulatory Genes Controlling Nodule Development in Pisum sativum L. // Plants. 2020. Vol. 9. No. 12. P. 1741. DOI: 10.3390/plants9121741 |
| [3] |
Shtark O, Provorov N, Mikić A, et al. Legume root symbioses: natural history and prospects for improvement. Ratar i Povrt. 2011;48:291–304. DOI: 10.5937/ratpov1102291S |
| [4] |
Shtark O., Provorov N., Mikić A., et al. Legume root symbioses: natural history and prospects for improvement // Ratar i Povrt. 2011. Vol. 48. P. 291–304. DOI: 10.5937/ratpov1102291S |
| [5] |
Tikhonovich IA, Andronov EE, Borisov AY, et al. The principle of genome complementarity in the enhancement of plant adaptive capacities. Russ J Genet. 2015;51:831–846. DOI: 10.1134/S1022795415090124 |
| [6] |
Tikhonovich I.A., Andronov E.E., Borisov A.Y., et al. The principle of genome complementarity in the enhancement of plant adaptive capacities // Russ J Genet. 2015. Vol. 51. P. 831–846. DOI: 10.1134/S1022795415090124 |
| [7] |
Zohary D, Hopf M. Domestication of Plants in the Old World: The origin and spread of domesticated plants in Southwest Asia, Europe, and the Mediterranean Basin. Published to Oxford Scholarship Online, 2000. Available from: https://oxford.universitypressscholarship.com/view/10.1093/acprof:osobl/9780199549061.001.0001/acprof- 9780199549061 |
| [8] |
Zohary D., Hopf M. Domestication of Plants in the Old World: The origin and spread of domesticated plants in Southwest Asia, Europe, and the Mediterranean Basin. Published to Oxford Scholarship Online, 2000. Доступ по ссылке: https://oxford.universitypressscholarship.com/view/10.1093/acprof: osobl/9780199549061.001.0001/acprof-9780199549061 |
| [9] |
Smýkal P, Coyne CJ, Redden R, et al. Genetic and Genomic Resour. Grain Legume Improvement. Elsevier, 2013. DOI: 10.1016/C2012-0-00217-7 |
| [10] |
Smýkal P., Coyne C.J., Redden R., et al. Genetic and Genomic Resour. Grain Legume Improvement. Elsevier, 2013. DOI: 10.1016/C2012-0-00217-7 |
| [11] |
Weeden NF. Genetic changes accompanying the domestication of Pisum sativum: is there a common genetic basis to the ‘domestication syndrome’ for legumes? Ann Bot. 2007;100(5): 1017–1025. DOI: 10.1093/aob/mcm122 |
| [12] |
Weeden N.F. Genetic changes accompanying the domestication of Pisum sativum: is there a common genetic basis to the ‘domestication syndrome’ for legumes? // Ann Bot. 2007. Vol. 100. P. No. 5. P. 1017–1025. DOI: 10.1093/aob/mcm122 |
| [13] |
Smýkal P, Nelson M, Berger J, Von E. Wettberg, The Impact of Genetic Changes during Crop Domestication. Agronomy. 2018;8(7);119. DOI: 10.3390/agronomy8070119 |
| [14] |
Smýkal P., Nelson M., Berger J., Von E. Wettberg, The Impact of Genetic Changes during Crop Domestication // Agronomy. 2018. Vol. 8. No. 7. P. 119. DOI: 10.3390/agronomy8070119 |
| [15] |
Shtark OY, Danilova TN, Naumkina TS, et al. Analysis of Pea (Pisum Sativum L.) Source Material for Breeding of Cultivars with High Symbiotic Potential and Choice of Criteria for Its Evaluation. Ecological genetics. 2006;4(2):22–28. (In Russ.) DOI: 10.17816/ecogen4222-28 |
| [16] |
Штарк О.Ю., Данилова Т.Н., Наумкина Т.С., и др. Анализ исходного материала гороха посевного (Pisum sativum L.) Для селекции сортов с высоким симбиотическим потенциалом и выбор параметров для его оценки // Экологическая генетика. 2006. Т. 4, № 2. С. 22–28. DOI: 10.17816/ecogen4222-28 |
| [17] |
Shtark OY, Borisov AY, Zhukov VA, Tikhonovich IA. Mutually beneficial legume symbioses with soil microbes and their potential for plant production. Symbiosis. 2012;58:51–62. DOI: 10.1007/s13199-013-0226-2 |
| [18] |
Shtark O.Y., Borisov A.Y., Zhukov V.A., Tikhonovich I.A. Mutually beneficial legume symbioses with soil microbes and their potential for plant production // Symbiosis. 2012. Vol. 58. P. 51–62. DOI: 10.1007/s13199-013-0226-2 |
| [19] |
Desalegn G, Turetschek R, Kaul H-P, Wienkoop S. Microbial symbionts affect Pisum sativum proteome and metabolome under Didymella pinodes infection. J Proteomics. 2016;143:173–187. DOI: 10.1016/J.JPROT.2016.03.018 |
| [20] |
Desalegn G., Turetschek R., Kaul H.-P., Wienkoop S. Microbial symbionts affect Pisum sativum proteome and metabolome under Didymella pinodes infection // J Proteomics. 2016. Vol. 143. P. 173–187. DOI: 10.1016/J.JPROT.2016.03.018 |
| [21] |
Ranjbar Sistani N, Kau H-P, Desalegn G, Wienkoop S. Rhizobium Impacts on Seed Productivity, Quality, and Protection of Pisum sativum upon Disease Stress Caused by Didymella pinodes: Phenotypic, Proteomic, and Metabolomic Traits. Front Plant Sci. 2017;8. DOI: 10.3389/fpls.2017.01961 |
| [22] |
Ranjbar Sistani N., Kau H.-P., Desalegn G., Wienkoop S. Rhizobium Impacts on Seed Productivity, Quality, and Protection of Pisum sativum upon Disease Stress Caused by Didymella pinodes: Phenotypic, Proteomic, and Metabolomic Traits // Front Plant Sci. 2017. Vol. 8. DOI: 10.3389/fpls.2017.01961 |
| [23] |
Mamontova T, Afonin AM, Ihling C, et al. Profiling of seed proteome in pea (Pisum Sativum L.) lines characterized with high and low responsivity to combined inoculation with nodule bacteria and arbuscular mycorrhizal fungi. Molecules. 2019;24(8):1603. DOI: 10.3390/molecules24081603 |
| [24] |
Mamontova T., Afonin A.M., Ihling C., et al. Profiling of seed proteome in pea (Pisum sativum L.) lines characterized with high and low responsivity to combined inoculation with nodule bacteria and arbuscular mycorrhizal fungi // Molecules. 2019. Vol. 24. No. 8. P. 1603. DOI: 10.3390/molecules24081603 |
| [25] |
Shtark OY, Zhukov VA, Puzanskiy RK, et al. Metabolic alterations in pea leaves during arbuscular mycorrhiza development. PeerJ. 2019. DOI: 10.7717/peerj.7495 |
| [26] |
Shtark O.Y., Zhukov V.A., Puzanskiy R.K., et al. Metabolic alterations in pea leaves during arbuscular mycorrhiza development // PeerJ. 2019. DOI: 10.7717/peerj.7495 |
| [27] |
Zhernakov AI, Shtark OY, Kulaeva OA, et al. Mapping-by-sequencing using NGS-based 3'-MACE-Seq reveals a new mutant allele of the essential nodulation gene Sym33 (IPD3) in pea (Pisum sativum L.). Peer J. 2019;7. DOI: 10.7717/peerj.6662 |
| [28] |
Zhernakov A.I., Shtark O.Y., Kulaeva O.A., et al. Mapping-by-sequencing using NGS-based 3'-MACE-Seq reveals a new mutant allele of the essential nodulation gene Sym33 (IPD3) in pea (Pisum sativum L.) // Peer J. 2019. Vol. 7. DOI: 10.7717/peerj.6662 |
| [29] |
Kozlova N, Strunnikova OK. Production and specificity of polyclonal antibodies against soluble proteins from the arbuscular mycorrhizal fungus Glomus intraradices. Mycorrhiza. 2001;10:301–305. DOI: 10.1007/PL00009999 |
| [30] |
Kozlova N., Strunnikova O.K. Production and specificity of polyclonal antibodies against soluble proteins from the arbuscular mycorrhizal fungus Glomus intraradices // Mycorrhiza. 2001. Vol. 10. P. 301–305. DOI: 10.1007/PL00009999 |
| [31] |
Afonin A, Sulima A, Zhernakov A, Zhukov V. Draft genome of the strain RCAM1026 Rhizobium leguminosarum bv. viciae. Genomics Data. 2017;11:85–86. DOI: 10.1016/j.gdata.2016.12.003 |
| [32] |
Afonin A., Sulima A., Zhernakov A., Zhukov V. Draft genome of the strain RCAM1026 Rhizobium leguminosarum bv. viciae // Genomics Data. 2017. Vol. 11. P. 85–86. DOI: 10.1016/j.gdata.2016.12.003 |
| [33] |
Zhukov VA, Shtark O, Tikhonovich IA. Evaluation of the symbiotic effectiveness of pea (Pisum sativum L.) Genotypes in pot experiment. Agric Biol. 2017;52:607–614. DOI: 10.15389/agrobiology.2017.3.607eng |
| [34] |
Zhukov V.A., Shtark O., Tikhonovich I.A. Evaluation of the symbiotic effectiveness of pea (Pisum sativum L.) genotypes in pot experiment // Agric Biol. 2017. Vol. 52. P. 607–614. DOI: 10.15389/agrobiology.2017.3.607eng |
| [35] |
Fehske H, Schneider R, Weiße A. Computational Many-Particle Physics. Springer, Berlin, Heidelber, 2008. DOI: 10.1007/978-3-540-74686-7 |
| [36] |
Fehske H., Schneider R., Weiße A. Computational Many-Particle Physics. Springer, Berlin, Heidelber, 2008. DOI: 10.1007/978-3-540-74686-7 |
| [37] |
Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32(19):3047–3048. DOI: 10.1093/bioinformatics/btw354 |
| [38] |
Ewels P., Magnusson M., Lundin S., Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report // Bioinformatics. 2016. Vol. 32. No. 19. P. 3047–3048. DOI: 10.1093/bioinformatics/btw354 |
| [39] |
Afonin AM, Leppyanen IV, Kulaeva OA, et al. A high coverage reference transcriptome assembly of pea (Pisum sativum L.) Mycorrhizal roots. Vavilov journal of genetics and breeding. 2020;24(4): 331–339. DOI: 10.18699/VJ20.625 |
| [40] |
Афонин А.М., Леппянен И.В., Кулаева О.А., и др. Референсный транскриптом микоризованных корней гороха посевного (Pisum sativum L.) с высоким покрытием // Вавиловский журнал генетики и селекции. 2020. Т. 24, № 4. С. 331–339. DOI: 10.18699/VJ20.625 |
| [41] |
Kreplak J, Madoui MA, Cápal P, et al. A reference genome for pea provides insight into legume genome evolution. Nat Genet. 2019;51:1411–1422. DOI: 10.1038/s41588-019-0480-1 |
| [42] |
Kreplak J., Madoui M.A., Cápal P, et al. A reference genome for pea provides insight into legume genome evolution // Nat Genet. 2019. Vol. 51. P. 1411–1422. DOI: 10.1038/s41588-019-0480-1 |
| [43] |
Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. DOI: 10.1093/bioinformatics/bts635 |
| [44] |
Dobin A., Davis C.A., Schlesinger F., et al. STAR: ultrafast universal RNA-seq aligner // Bioinformatics. 2013. Vol. 29. No. 1. P. 15–21. DOI: 10.1093/bioinformatics/bts635 |
| [45] |
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. DOI:10.1186/s13059-014-0550-8 |
| [46] |
Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 // Genome Biol. 2014. Vol. 15. ID550. DOI:10.1186/s13059-014-0550-8 |
| [47] |
Lohse M, Nagel A, Herter T, et al. Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant, Cell Environ. 2014;37(5):1250–1258. DOI: 10.1111/pce.12231 |
| [48] |
Lohse M., Nagel A., Herter T., et al. Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data // Plant, Cell Environ. 2014. Vol. 37. No. 5. P. 1250–1258. DOI: 10.1111/pce.12231 |
| [49] |
Poplin R, Chang PC, Alexander D, et al. A universal snp and small-indel variant caller using deep neural networks. Nat Biotechnol. 2018;36:983–987. DOI: 10.1038/nbt.4235 |
| [50] |
Poplin R., Chang P.C., Alexander D., et al. A universal snp and small-indel variant caller using deep neural networks // Nat Biotechnol. 2018. Vol. 36. P. 983–987. DOI: 10.1038/nbt.4235 |
| [51] |
Lin MF, Rodeh O, Penn J, et al. GLnexus: joint variant calling for large cohort sequencing. BioRxiv. 2018:343970. DOI: 10.1101/343970 |
| [52] |
Lin M.F., Rodeh O., Penn J., et al. GLnexus: joint variant calling for large cohort sequencing // BioRxiv. 2018. ID343970. DOI: 10.1101/343970 |
| [53] |
Knaus BJ, Grünwald NJ. VCFR: a package to manipulate and visualize variant call format data in R. Mol Ecol Resour. 2017;17: 44–53. DOI: 10.1111/1755-0998.12549 |
| [54] |
Knaus B.J., Grünwald N.J. VCFR: a package to manipulate and visualize variant call format data in R // Mol Ecol Resour. 2017. Vol. 17. P. 44–53. DOI: 10.1111/1755-0998.12549 |
| [55] |
Jombart T. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403–1405. DOI: 10.1093/bioinformatics/btn129 |
| [56] |
Jombart T. adegenet: a R package for the multivariate analysis of genetic markers // Bioinformatics. 2008. Vol. 24. No. 11. P. 1403–1405. DOI: 10.1093/bioinformatics/btn129 |
| [57] |
Kamvar ZN, Brooks JC, Grünwald NJ. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front Genet. 2015;6. DOI: 10.3389/fgene.2015.00208 |
| [58] |
Kamvar Z.N., Brooks J.C., Grünwald N.J. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality // Front Genet. 2015. Vol. 6. DOI: 10.3389/fgene.2015.00208 |
| [59] |
Ribeiro CW, Baldacci-Cresp F, Pierre O, Rouhier N. Regulation of Differentiation of Nitrogen-Fixing Bacteria by Microsymbiont Targeting of Plant Thioredoxin s1. Curr Biol. 2017;27(2):250–256. DOI: 10.1016/j.cub.2016.11.013 |
| [60] |
Ribeiro C.W., Baldacci-Cresp F., Pierre O., Rouhier N. Regulation of Differentiation of Nitrogen-Fixing Bacteria by Microsymbiont Targeting of Plant Thioredoxin s1 // Curr Biol. 2017. Vol. 27. No. 2. P. 250–256. DOI: 10.1016/j.cub.2016.11.013 |
| [61] |
Kuhn H, Küster H, Requena N. Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytol. 2010;185(3):716–733. DOI: 10.1111/j.1469-8137.2009.03116.x |
| [62] |
Kuhn H., Küster H., Requena N. Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula // New Phytol. 2010. Vol. 185. No. 3. P. 716–733. DOI: 10.1111/j.1469-8137.2009.03116.x |
| [63] |
von Sivers L, Jaspar H, Johst B, et al. Brassinosteroids Affect the Symbiosis Between the AM Fungus rhizoglomus irregularis and Solanaceous Host Plants. Front Plant Sci. 2019;10:571 DOI: 10.3389/fpls.2019.00571 |
| [64] |
von Sivers L., Jaspar H., Johst B., et al. Brassinosteroids Affect the Symbiosis Between the AM Fungus Rhizoglomus irregularis and Solanaceous Host Plants // Front Plant Sci. 2019. Vol. 10. P. 571. DOI: 10.3389/fpls.2019.00571 |
| [65] |
Melo PM, Lima LM, Santos IM, et al. Expression of the plastid-located glutamine synthetase of Medicago truncatula. Accumulation of the precursor in root nodules reveals an in vivo control at the level of protein import into plastids. Plant Physiol. 2003;132(1):390–399. DOI: 10.1104/pp.102.016675 |
| [66] |
Melo P.M., Lima L.M., Santos I.M., et al. Expression of the plastid-located glutamine synthetase of Medicago truncatula. Accumulation of the precursor in root nodules reveals an in vivo control at the level of protein import into plastids // Plant Physiol. 2003. Vol. 132. No. 1. P. 390–399. DOI: 10.1104/pp.102.016675 |
| [67] |
García-Calderón M, Chiurazzi M, Espuny MR, Márquez AJ. Photorespiratory metabolism and nodule function: Behavior of Lotus japonicus mutants deficient in plastid glutamine synthetase. Mol Plant-Microbe Interact. 2012;25(2):211–219. DOI: 10.1094/MPMI-07-11-0200 |
| [68] |
García-Calderón M., Chiurazzi M., Espuny M.R., Márquez A.J. Photorespiratory metabolism and nodule function: Behavior of Lotus japonicus mutants deficient in plastid glutamine synthetase // Mol Plant-Microbe Interact. 2012. Vol. 25. No. 2. P. 211–219. DOI: 10.1094/MPMI-07-11-0200 |
| [69] |
Stauder R, Welsch R, Camagna M, et al. Strigolactone Levels in Dicot Roots Are Determined by an Ancestral Symbiosis-Regulated Clade of the PHYTOENE SYNTHASE Gene Family. Front Plant Sci. 2018;9. DOI: 10.3389/fpls.2018.00255 |
| [70] |
Stauder R., Welsch R., Camagna M., et al. Strigolactone Levels in Dicot Roots Are Determined by an Ancestral Symbiosis-Regulated Clade of the PHYTOENE SYNTHASE Gene Family // Front Plant Sci. 2018. Vol. 9. DOI: 10.3389/fpls.2018.00255 |
| [71] |
Waters MT, Gutjahr C, Bennett T, Nelson DC. Strigolactone Signaling and Evolution. Annu Rev Plant Biol. 2017;68:291–322. DOI: 10.1146/annurev-arplant-042916-040925 |
| [72] |
Waters M.T., Gutjahr C., Bennett T., Nelson D.C. Strigolactone Signaling and Evolution // Annu Rev Plant Biol. 2017. Vol. 68. P. 291–322. DOI: 10.1146/annurev-arplant-042916-040925 |
| [73] |
Tang H, Krishnakumar V, Bidwell S, et al. An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics. 2014;15:312. DOI: 10.1186/1471-2164-15-312 |
| [74] |
Tang H., Krishnakumar V., Bidwell S., et al. An improved genome release (version Mt4.0) for the model legume Medicago truncatula // BMC Genomics. 2014. Vol. 15. ID312. DOI: 10.1186/1471-2164-15-312 |
| [75] |
Klimmek F, Sjödin A, Noutsos C, et al. Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol. 2006;140(3);793–804. DOI: 10.1104/pp.105.073304 |
| [76] |
Klimmek F., Sjödin A., Noutsos C., et al. Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants // Plant Physiol. 2006. Vol. 140. No. 3. P. 793–804. DOI: 10.1104/pp.105.073304 |
| [77] |
Marzec M. Perception and signaling of strigolactones. Front Plant Sci. 2016;7:1260. DOI: 10.3389/fpls.2016.01260 |
| [78] |
Marzec M. Perception and signaling of strigolactones // Front Plant Sci. 2016. Vol. 7. ID1260. DOI: 10.3389/fpls.2016.01260 |
| [79] |
Keymer A, Pimprikar P, Wewer V, et al. Lipid transfer from plants to arbuscular mycorrhiza fungi. Elife. 2017;6. DOI: 10.7554/eLife.29107 |
| [80] |
Keymer A., Pimprikar P., Wewer V., et al. Lipid transfer from plants to arbuscular mycorrhiza fungi // Elife. 2017. Vol. 6. DOI: 10.7554/eLife.29107 |
| [81] |
Bravo A, Brands M, Wewer V, et al. Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytol. 2017;214(4):1631–1645. DOI: 10.1111/nph.14533 |
| [82] |
Bravo A., Brands M., Wewer V., et al. Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza // New Phytol. 2017. Vol. 214. No. 4. P. 1631–1645. DOI: 10.1111/nph.14533 |
| [83] |
Abdel-Lateif K, Bogusz D, Hocher V. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav. 2012;7(6):636–641. DOI: 10.4161/psb.20039 |
| [84] |
Abdel-Lateif K., Bogusz D., Hocher V. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria // Plant Signal Behav. 2012. Vol. 7. No. 6. P. 636–641. DOI: 10.4161/psb.20039 |
| [85] |
Wang P, Hawes C, Hussey PJ. Plant Endoplasmic Reticulum–Plasma Membrane Contact Sites. Trends Plant Sci. 2017;22(4): 289–297. DOI: 10.1016/j.tplants.2016.11.008 |
| [86] |
Wang P., Hawes C., Hussey P.J. Plant Endoplasmic Reticulum–Plasma Membrane Contact Sites // Trends Plant Sci. 2017. Vol. 22. No. 4. P. 289–297. DOI: 10.1016/j.tplants.2016.11.008 |
| [87] |
Genre A, Chabaud M, Faccio A, et al. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell. 2008;20(5):1407–1420. DOI: 10.1105/tpc.108.059014 |
| [88] |
Genre A., Chabaud M., Faccio A., et al. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota // Plant Cell. 2008. Vol. 20. No. 5. P. 1407–1420. DOI: 10.1105/tpc.108.059014 |
| [89] |
Dao TTH, Linthorst HJM, Verpoorte R. Chalcone synthase and its functions in plant resistance. Phytochem Rev. 2011;10:397–412. DOI: 10.1007/s11101-011-9211-7 |
| [90] |
Dao T.T.H., Linthorst H.J.M., Verpoorte R. Chalcone synthase and its functions in plant resistance // Phytochem Rev. 2011. Vol. 10. P. 397–412. DOI: 10.1007/s11101-011-9211-7 |
| [91] |
Mierziak J, Wojtasik W, Kulma A, et al. 3-Hydroxybutyrate Is Active Compound in Flax that Upregulates Genes Involved in DNA Methylation. Int J Mol Sci. 2020;21(8):2887. DOI: 10.3390/ijms21082887 |
| [92] |
Mierziak J., Wojtasik W., Kulma A., et al. 3-Hydroxybutyrate Is Active Compound in Flax that Upregulates Genes Involved in DNA Methylation // Int J Mol Sci. 2020. Vol. 21. No. 8. P. 2887. DOI: 10.3390/ijms21082887 |
| [93] |
Chen T, Duan L, Zhou B, et al. Interplay of Pathogen-Induced Defense Responses and Symbiotic Establishment in Medicago truncatula. Front Microbiol. 2017;8:973. DOI: 10.3389/fmicb.2017.00973 |
| [94] |
Chen T., Duan L., Zhou B., et al. Interplay of Pathogen-Induced Defense Responses and Symbiotic Establishment in Medicago truncatula // Front Microbiol. 2017. Vol. 8. P. 973. DOI: 10.3389/fmicb.2017.00973 |
| [95] |
Lenser T, Theißen G. Molecular mechanisms involved in convergent crop domestication. Trends Plant Sci. 2013;18(12):704–714. DOI: 10.1016/j.tplants.2013.08.007 |
| [96] |
Lenser T., Theißen G. Molecular mechanisms involved in convergent crop domestication // Trends Plant Sci. 2013. Vol. 18. No. 12. P. 704–714. DOI: 10.1016/j.tplants.2013.08.007 |
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