Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency

Maryam Nasr Esfahani, Komaki Inoue, Ha Duc Chu, Kien Huu Nguyen, Chien Van Ha, Yasuko Watanabe, David J. Burritt, Luis Herrera-Estrella, Keiichi Mochida, Lam Son Phan Tran

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Phosphate (Pi) deficiency is known to be a major limitation for symbiotic nitrogen fixation (SNF), and hence legume crop productivity globally. However, very little information is available on the adaptive mechanisms, particularly in the important legume crop chickpea (Cicer arietinum L.), which enable nodules to respond to low-Pi availability. Thus, to elucidate these mechanisms in chickpea nodules at molecular level, we used an RNA sequencing approach to investigate transcriptomes of the nodules in Mesorhizobium mediterraneum SWRI9–(MmSWRI9)–chickpea and M. ciceri CP-31–(McCP-31)–chickpea associations under Pi-sufficient and Pi-deficient conditions, of which the McCP-31–chickpea association has a better SNF capacity than the MmSWRI9–chickpea association during Pi starvation. Our investigation revealed that more genes showed altered expression patterns in MmSWRI9-induced nodules than in McCP-31-induced nodules (540 vs. 225) under Pi deficiency, suggesting that the Pi-starvation-more-sensitive MmSWRI9-induced nodules required expression change in a larger number of genes to cope with low-Pi stress than the Pi-starvation-less-sensitive McCP-31-induced nodules. The functional classification of differentially expressed genes (DEGs) was examined to gain an understanding of how chickpea nodules respond to Pi starvation, caused by soil Pi deficiency. As a result, more DEGs involved in nodulation, detoxification, nutrient/ion transport, transcriptional factors, key metabolic pathways, Pi remobilization and signalling were found in Pi-starved MmSWRI9-induced nodules than in Pi-starved McCP-31-induced nodules. Our findings have enabled the identification of molecular processes that play important roles in the acclimation of nodules to Pi deficiency, ultimately leading to the development of Pi-efficient chickpea symbiotic associations suitable for Pi-deficient soils.

Original languageEnglish
Pages (from-to)911-926
Number of pages16
JournalPlant Journal
Volume91
Issue number5
DOIs
Publication statusPublished - Sep 1 2017

Fingerprint

Mesorhizobium mediterraneum
Cicer
Gene Expression Profiling
transcriptomics
starvation
Mesorhizobium
Phosphates
phosphates
Starvation
nitrogen fixation
genes
legumes
Nitrogen Fixation
Fabaceae
ion transport
Cicer arietinum
Genes
crops
nodulation
transcriptome

Keywords

  • Cicer arietinum
  • Mesorhizobium ciceri
  • Mesorhizobium mediterraneum
  • phosphate deficiency
  • symbiotic nitrogen fixation
  • transcriptome analysis

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency. / Nasr Esfahani, Maryam; Inoue, Komaki; Chu, Ha Duc; Nguyen, Kien Huu; Van Ha, Chien; Watanabe, Yasuko; Burritt, David J.; Herrera-Estrella, Luis; Mochida, Keiichi; Tran, Lam Son Phan.

In: Plant Journal, Vol. 91, No. 5, 01.09.2017, p. 911-926.

Research output: Contribution to journalArticle

Nasr Esfahani, M, Inoue, K, Chu, HD, Nguyen, KH, Van Ha, C, Watanabe, Y, Burritt, DJ, Herrera-Estrella, L, Mochida, K & Tran, LSP 2017, 'Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency', Plant Journal, vol. 91, no. 5, pp. 911-926. https://doi.org/10.1111/tpj.13616
Nasr Esfahani, Maryam ; Inoue, Komaki ; Chu, Ha Duc ; Nguyen, Kien Huu ; Van Ha, Chien ; Watanabe, Yasuko ; Burritt, David J. ; Herrera-Estrella, Luis ; Mochida, Keiichi ; Tran, Lam Son Phan. / Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency. In: Plant Journal. 2017 ; Vol. 91, No. 5. pp. 911-926.
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abstract = "Phosphate (Pi) deficiency is known to be a major limitation for symbiotic nitrogen fixation (SNF), and hence legume crop productivity globally. However, very little information is available on the adaptive mechanisms, particularly in the important legume crop chickpea (Cicer arietinum L.), which enable nodules to respond to low-Pi availability. Thus, to elucidate these mechanisms in chickpea nodules at molecular level, we used an RNA sequencing approach to investigate transcriptomes of the nodules in Mesorhizobium mediterraneum SWRI9–(MmSWRI9)–chickpea and M. ciceri CP-31–(McCP-31)–chickpea associations under Pi-sufficient and Pi-deficient conditions, of which the McCP-31–chickpea association has a better SNF capacity than the MmSWRI9–chickpea association during Pi starvation. Our investigation revealed that more genes showed altered expression patterns in MmSWRI9-induced nodules than in McCP-31-induced nodules (540 vs. 225) under Pi deficiency, suggesting that the Pi-starvation-more-sensitive MmSWRI9-induced nodules required expression change in a larger number of genes to cope with low-Pi stress than the Pi-starvation-less-sensitive McCP-31-induced nodules. The functional classification of differentially expressed genes (DEGs) was examined to gain an understanding of how chickpea nodules respond to Pi starvation, caused by soil Pi deficiency. As a result, more DEGs involved in nodulation, detoxification, nutrient/ion transport, transcriptional factors, key metabolic pathways, Pi remobilization and signalling were found in Pi-starved MmSWRI9-induced nodules than in Pi-starved McCP-31-induced nodules. Our findings have enabled the identification of molecular processes that play important roles in the acclimation of nodules to Pi deficiency, ultimately leading to the development of Pi-efficient chickpea symbiotic associations suitable for Pi-deficient soils.",
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AU - Van Ha, Chien

AU - Watanabe, Yasuko

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AU - Mochida, Keiichi

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N2 - Phosphate (Pi) deficiency is known to be a major limitation for symbiotic nitrogen fixation (SNF), and hence legume crop productivity globally. However, very little information is available on the adaptive mechanisms, particularly in the important legume crop chickpea (Cicer arietinum L.), which enable nodules to respond to low-Pi availability. Thus, to elucidate these mechanisms in chickpea nodules at molecular level, we used an RNA sequencing approach to investigate transcriptomes of the nodules in Mesorhizobium mediterraneum SWRI9–(MmSWRI9)–chickpea and M. ciceri CP-31–(McCP-31)–chickpea associations under Pi-sufficient and Pi-deficient conditions, of which the McCP-31–chickpea association has a better SNF capacity than the MmSWRI9–chickpea association during Pi starvation. Our investigation revealed that more genes showed altered expression patterns in MmSWRI9-induced nodules than in McCP-31-induced nodules (540 vs. 225) under Pi deficiency, suggesting that the Pi-starvation-more-sensitive MmSWRI9-induced nodules required expression change in a larger number of genes to cope with low-Pi stress than the Pi-starvation-less-sensitive McCP-31-induced nodules. The functional classification of differentially expressed genes (DEGs) was examined to gain an understanding of how chickpea nodules respond to Pi starvation, caused by soil Pi deficiency. As a result, more DEGs involved in nodulation, detoxification, nutrient/ion transport, transcriptional factors, key metabolic pathways, Pi remobilization and signalling were found in Pi-starved MmSWRI9-induced nodules than in Pi-starved McCP-31-induced nodules. Our findings have enabled the identification of molecular processes that play important roles in the acclimation of nodules to Pi deficiency, ultimately leading to the development of Pi-efficient chickpea symbiotic associations suitable for Pi-deficient soils.

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