Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
Understanding the beneficial plant–microbe interactions is becoming extremely critical for deploying microbes imparting plant fitness and achieving sustainability in agriculture. Diazotrophic bacteria have the unique ability to survive without external sources of nitrogen and simultaneously promote...
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| Format: | Article |
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Frontiers Media S.A.
2022-11-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.939395/full |
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| author | Manish Ranjan Saini Manish Ranjan Saini Latha P. Chandran Kalyani Makarand Barbadikar Amitha Mithra V. Sevanthi Gautam Chawla Megha Kaushik Ekta Mulani Amol Sarjerao Phule Rajani Govindannagari Bandeppa Sonth Subodh Kumar Sinha Raman Meenakshi Sundaram Pranab Kumar Mandal |
| author_facet | Manish Ranjan Saini Manish Ranjan Saini Latha P. Chandran Kalyani Makarand Barbadikar Amitha Mithra V. Sevanthi Gautam Chawla Megha Kaushik Ekta Mulani Amol Sarjerao Phule Rajani Govindannagari Bandeppa Sonth Subodh Kumar Sinha Raman Meenakshi Sundaram Pranab Kumar Mandal |
| author_sort | Manish Ranjan Saini |
| collection | DOAJ |
| description | Understanding the beneficial plant–microbe interactions is becoming extremely critical for deploying microbes imparting plant fitness and achieving sustainability in agriculture. Diazotrophic bacteria have the unique ability to survive without external sources of nitrogen and simultaneously promote host plant growth, but the mechanisms of endophytic interaction in cereals and legumes have not been studied extensively. We have studied the early interaction of two diazotrophic bacteria, Gluconacetobacter diazotrophicus (GAB) and Bradyrhizobium japonicum (BRH), in 15-day-old seedlings of rice and soybean up to 120 h after inoculation (hai) under low-nitrogen medium. Root colonization of GAB in rice was higher than that of BRH, and BRH colonization was higher in soybean roots as observed from the scanning electron microscopy at 120 hai. Peroxidase enzyme was significantly higher at 24 hai but thereafter was reduced sharply in soybean and gradually in rice. The roots of rice and soybean inoculated with GAB and BRH harvested from five time points were pooled, and transcriptome analysis was executed along with control. Two pathways, “Plant pathogen interaction” and “MAPK signaling,” were specific to Rice-Gluconacetobacter (RG), whereas the pathways related to nitrogen metabolism and plant hormone signaling were specific to Rice-Bradyrhizobium (RB) in rice. Comparative transcriptome analysis of the root tissues revealed that several plant–diazotroph-specific differentially expressed genes (DEGs) and metabolic pathways of plant–diazotroph-specific transcripts, viz., chitinase, brassinosteroid, auxin, Myeloblastosis (MYB), nodulin, and nitrate transporter (NRT), were common in all plant–diazotroph combinations; three transcripts, viz., nitrate transport accessory protein (NAR), thaumatin, and thionin, were exclusive in rice and another three transcripts, viz., NAC (NAM: no apical meristem, ATAF: Arabidopsis thaliana activating factor, and CUC: cup-shaped cotyledon), ABA (abscisic acid), and ammonium transporter, were exclusive in soybean. Differential expression of these transcripts and reduction in pathogenesis-related (PR) protein expression show the early interaction. Based on the interaction, it can be inferred that the compatibility of rice and soybean is more with GAB and BRH, respectively. We propose that rice is unable to identify the diazotroph as a beneficial microorganism or a pathogen from an early response. So, it expressed the hypersensitivity-related transcripts along with PR proteins. The molecular mechanism of diazotrophic associations of GAB and BRH with rice vis-à-vis soybean will shed light on the basic understanding of host responses to beneficial microorganisms. |
| first_indexed | 2024-04-11T06:38:11Z |
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| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-11T06:38:11Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-874f1002bd6e421aaebee8c07e1292212022-12-22T04:39:38ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.939395939395Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysisManish Ranjan Saini0Manish Ranjan Saini1Latha P. Chandran2Kalyani Makarand Barbadikar3Amitha Mithra V. Sevanthi4Gautam Chawla5Megha Kaushik6Ekta Mulani7Amol Sarjerao Phule8Rajani Govindannagari9Bandeppa Sonth10Subodh Kumar Sinha11Raman Meenakshi Sundaram12Pranab Kumar Mandal13Indian Council of Agricultural Research (ICAR) National Institute for Plant Biotechnology, New Delhi, IndiaKalinga Institute of Industrial Technology (KIIT) School of Biotechnology, KIIT University, Bhubaneswar, IndiaICAR-Indian Institute of Rice Research, Hyderabad, IndiaICAR-Indian Institute of Rice Research, Hyderabad, IndiaIndian Council of Agricultural Research (ICAR) National Institute for Plant Biotechnology, New Delhi, IndiaDivision of Nematology, ICAR- Indian Agriculture Research Institute, New Delhi, IndiaIndian Council of Agricultural Research (ICAR) National Institute for Plant Biotechnology, New Delhi, IndiaIndian Council of Agricultural Research (ICAR) National Institute for Plant Biotechnology, New Delhi, IndiaICAR-Indian Institute of Rice Research, Hyderabad, IndiaICAR-Indian Institute of Rice Research, Hyderabad, IndiaICAR-Indian Institute of Rice Research, Hyderabad, IndiaIndian Council of Agricultural Research (ICAR) National Institute for Plant Biotechnology, New Delhi, IndiaICAR-Indian Institute of Rice Research, Hyderabad, IndiaIndian Council of Agricultural Research (ICAR) National Institute for Plant Biotechnology, New Delhi, IndiaUnderstanding the beneficial plant–microbe interactions is becoming extremely critical for deploying microbes imparting plant fitness and achieving sustainability in agriculture. Diazotrophic bacteria have the unique ability to survive without external sources of nitrogen and simultaneously promote host plant growth, but the mechanisms of endophytic interaction in cereals and legumes have not been studied extensively. We have studied the early interaction of two diazotrophic bacteria, Gluconacetobacter diazotrophicus (GAB) and Bradyrhizobium japonicum (BRH), in 15-day-old seedlings of rice and soybean up to 120 h after inoculation (hai) under low-nitrogen medium. Root colonization of GAB in rice was higher than that of BRH, and BRH colonization was higher in soybean roots as observed from the scanning electron microscopy at 120 hai. Peroxidase enzyme was significantly higher at 24 hai but thereafter was reduced sharply in soybean and gradually in rice. The roots of rice and soybean inoculated with GAB and BRH harvested from five time points were pooled, and transcriptome analysis was executed along with control. Two pathways, “Plant pathogen interaction” and “MAPK signaling,” were specific to Rice-Gluconacetobacter (RG), whereas the pathways related to nitrogen metabolism and plant hormone signaling were specific to Rice-Bradyrhizobium (RB) in rice. Comparative transcriptome analysis of the root tissues revealed that several plant–diazotroph-specific differentially expressed genes (DEGs) and metabolic pathways of plant–diazotroph-specific transcripts, viz., chitinase, brassinosteroid, auxin, Myeloblastosis (MYB), nodulin, and nitrate transporter (NRT), were common in all plant–diazotroph combinations; three transcripts, viz., nitrate transport accessory protein (NAR), thaumatin, and thionin, were exclusive in rice and another three transcripts, viz., NAC (NAM: no apical meristem, ATAF: Arabidopsis thaliana activating factor, and CUC: cup-shaped cotyledon), ABA (abscisic acid), and ammonium transporter, were exclusive in soybean. Differential expression of these transcripts and reduction in pathogenesis-related (PR) protein expression show the early interaction. Based on the interaction, it can be inferred that the compatibility of rice and soybean is more with GAB and BRH, respectively. We propose that rice is unable to identify the diazotroph as a beneficial microorganism or a pathogen from an early response. So, it expressed the hypersensitivity-related transcripts along with PR proteins. The molecular mechanism of diazotrophic associations of GAB and BRH with rice vis-à-vis soybean will shed light on the basic understanding of host responses to beneficial microorganisms.https://www.frontiersin.org/articles/10.3389/fpls.2022.939395/fullGluconacetobacter diazotrophicusBradyrhizobium japonicumricesoybeanRNA-seqnitrogen fixation |
| spellingShingle | Manish Ranjan Saini Manish Ranjan Saini Latha P. Chandran Kalyani Makarand Barbadikar Amitha Mithra V. Sevanthi Gautam Chawla Megha Kaushik Ekta Mulani Amol Sarjerao Phule Rajani Govindannagari Bandeppa Sonth Subodh Kumar Sinha Raman Meenakshi Sundaram Pranab Kumar Mandal Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis Frontiers in Plant Science Gluconacetobacter diazotrophicus Bradyrhizobium japonicum rice soybean RNA-seq nitrogen fixation |
| title | Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis |
| title_full | Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis |
| title_fullStr | Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis |
| title_full_unstemmed | Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis |
| title_short | Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis |
| title_sort | understanding plant microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis |
| topic | Gluconacetobacter diazotrophicus Bradyrhizobium japonicum rice soybean RNA-seq nitrogen fixation |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.939395/full |
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