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Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.

Høgslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, Goffard N, Sanchez DH, Lippold F, Ott T, Sato S, Tabata S, Liboriussen P, Lohmann GV, Schauser L, Weiller GF, Udvardi MK, Stougaard J - PLoS ONE (2009)

Bottom Line: Another surprise was the extensive transcriptional response in whole root compared to the susceptible root zone where the cellular response is most pronounced.A large number of transcripts predicted to encode transcriptional regulators, receptors and proteins involved in signal transduction, as well as many genes with unknown function, were found to be regulated during nodule organogenesis and rhizobial infection.The complete data set was organized into an indexed expression directory that is accessible from a resource database, and here we present selected examples of biological questions that can be addressed with this comprehensive and powerful gene expression data set.

View Article: PubMed Central - PubMed

Affiliation: Centre for Carbohydrate Recognition and Signalling, MBI, Aarhus University, Aarhus C, Denmark.

ABSTRACT
Genetic analyses of plant symbiotic mutants has led to the identification of key genes involved in Rhizobium-legume communication as well as in development and function of nitrogen fixing root nodules. However, the impact of these genes in coordinating the transcriptional programs of nodule development has only been studied in limited and isolated studies. Here, we present an integrated genome-wide analysis of transcriptome landscapes in Lotus japonicus wild-type and symbiotic mutant plants. Encompassing five different organs, five stages of the sequentially developed determinate Lotus root nodules, and eight mutants impaired at different stages of the symbiotic interaction, our data set integrates an unprecedented combination of organ- or tissue-specific profiles with mutant transcript profiles. In total, 38 different conditions sampled under the same well-defined growth regimes were included. This comprehensive analysis unravelled new and unexpected patterns of transcriptional regulation during symbiosis and organ development. Contrary to expectations, none of the previously characterized nodulins were among the 37 genes specifically expressed in nodules. Another surprise was the extensive transcriptional response in whole root compared to the susceptible root zone where the cellular response is most pronounced. A large number of transcripts predicted to encode transcriptional regulators, receptors and proteins involved in signal transduction, as well as many genes with unknown function, were found to be regulated during nodule organogenesis and rhizobial infection. Combining wild type and mutant profiles of these transcripts demonstrates the activation of a complex genetic program that delineates symbiotic nitrogen fixation. The complete data set was organized into an indexed expression directory that is accessible from a resource database, and here we present selected examples of biological questions that can be addressed with this comprehensive and powerful gene expression data set.

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Transcript regulation by nitrate in Lotus.A) The pattern of IDs found to be regulated by nitrate and M. loti inoculation (1 dpi to 21 dpi). B) The pattern of IDs regulated by nitrate and M. loti inoculation (21 dpi). C) Number of IDs down-regulated (green), up-regulated (red) or differently regulated (black) by nitrate in Lotus roots and shoots when compared to untreated corresponding tissues. (R-M. loti, N-nitrate) PTR-peptide transporter; PEROX-peroxidase; CDPK-calcium and calmodulin kinase; U-unknown; TXA-TXA synthase; LRR-leucine rich repeat protein; GT-UDP- glycosyltransferase; TF-transcription factor; ARR8-response regulator 8; OTR-ornithine transporter; OX-oxidoreductase; GLRX-glutaredoxin; UTR-urea transporter; CYP-Cytochrome P450; ATP-ATPase; LSYN-lupeol synthase; STR-sugar transporter; ZNF-zinc finger; LY-lyase; PK-protein kinase; LCAR-L-carbamoylase; N21-nodulin 21; GDP-glycerophosphoryl diester phosphodiesterase; G3PTR-G-3-P transporter; PP-phosphatase; TDE-tumor differently expressed; SRG-senescence related gene; PEPC-phosphoenolpyruvate carboxylase; VTR-vacuolar transporter; SPI-serine protease inhibitor).
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pone-0006556-g005: Transcript regulation by nitrate in Lotus.A) The pattern of IDs found to be regulated by nitrate and M. loti inoculation (1 dpi to 21 dpi). B) The pattern of IDs regulated by nitrate and M. loti inoculation (21 dpi). C) Number of IDs down-regulated (green), up-regulated (red) or differently regulated (black) by nitrate in Lotus roots and shoots when compared to untreated corresponding tissues. (R-M. loti, N-nitrate) PTR-peptide transporter; PEROX-peroxidase; CDPK-calcium and calmodulin kinase; U-unknown; TXA-TXA synthase; LRR-leucine rich repeat protein; GT-UDP- glycosyltransferase; TF-transcription factor; ARR8-response regulator 8; OTR-ornithine transporter; OX-oxidoreductase; GLRX-glutaredoxin; UTR-urea transporter; CYP-Cytochrome P450; ATP-ATPase; LSYN-lupeol synthase; STR-sugar transporter; ZNF-zinc finger; LY-lyase; PK-protein kinase; LCAR-L-carbamoylase; N21-nodulin 21; GDP-glycerophosphoryl diester phosphodiesterase; G3PTR-G-3-P transporter; PP-phosphatase; TDE-tumor differently expressed; SRG-senescence related gene; PEPC-phosphoenolpyruvate carboxylase; VTR-vacuolar transporter; SPI-serine protease inhibitor).

Mentions: Compared to the rhizobia-inoculated roots, acclimation to nitrate as nitrogen source leads to regulation of a limited number of genes in Lotus. Genes corresponding to only 230 IDs were found differently regulated in the nitrate-grown roots compared to untreated roots, and out of these only 90 were specific for the nitrate treatment and were not found in the pool of genes regulated in response to M. loti. These included homologs of nitrate, peptide- and phosphate-transporters that were previously found regulated in Arabidopsis in response to inorganic nitrogen (reviewed in [67]). Interestingly, nine of the genes that were regulated by inoculation with M. loti were regulated similarly in the nitrate grown roots. Among these, genes encoding an UDP-glycosyltransferase and ARR8 are found, indicating that cytokinin signalling may be important in both symbiotic and inorganic nitrogen plant nutrition (Figure 5A and Folder S7). Not surprisingly, nitrate-grown roots have more differentially expressed genes in common with the 21 dpi roots, compared to the other analyzed time points. These included genes for anthocyanidin synthase and a urea transporter, which were down-regulated, and a couple of transcriptional regulators and N21, which were up-regulated (Figure 5B).


Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.

Høgslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, Goffard N, Sanchez DH, Lippold F, Ott T, Sato S, Tabata S, Liboriussen P, Lohmann GV, Schauser L, Weiller GF, Udvardi MK, Stougaard J - PLoS ONE (2009)

Transcript regulation by nitrate in Lotus.A) The pattern of IDs found to be regulated by nitrate and M. loti inoculation (1 dpi to 21 dpi). B) The pattern of IDs regulated by nitrate and M. loti inoculation (21 dpi). C) Number of IDs down-regulated (green), up-regulated (red) or differently regulated (black) by nitrate in Lotus roots and shoots when compared to untreated corresponding tissues. (R-M. loti, N-nitrate) PTR-peptide transporter; PEROX-peroxidase; CDPK-calcium and calmodulin kinase; U-unknown; TXA-TXA synthase; LRR-leucine rich repeat protein; GT-UDP- glycosyltransferase; TF-transcription factor; ARR8-response regulator 8; OTR-ornithine transporter; OX-oxidoreductase; GLRX-glutaredoxin; UTR-urea transporter; CYP-Cytochrome P450; ATP-ATPase; LSYN-lupeol synthase; STR-sugar transporter; ZNF-zinc finger; LY-lyase; PK-protein kinase; LCAR-L-carbamoylase; N21-nodulin 21; GDP-glycerophosphoryl diester phosphodiesterase; G3PTR-G-3-P transporter; PP-phosphatase; TDE-tumor differently expressed; SRG-senescence related gene; PEPC-phosphoenolpyruvate carboxylase; VTR-vacuolar transporter; SPI-serine protease inhibitor).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2717213&req=5

pone-0006556-g005: Transcript regulation by nitrate in Lotus.A) The pattern of IDs found to be regulated by nitrate and M. loti inoculation (1 dpi to 21 dpi). B) The pattern of IDs regulated by nitrate and M. loti inoculation (21 dpi). C) Number of IDs down-regulated (green), up-regulated (red) or differently regulated (black) by nitrate in Lotus roots and shoots when compared to untreated corresponding tissues. (R-M. loti, N-nitrate) PTR-peptide transporter; PEROX-peroxidase; CDPK-calcium and calmodulin kinase; U-unknown; TXA-TXA synthase; LRR-leucine rich repeat protein; GT-UDP- glycosyltransferase; TF-transcription factor; ARR8-response regulator 8; OTR-ornithine transporter; OX-oxidoreductase; GLRX-glutaredoxin; UTR-urea transporter; CYP-Cytochrome P450; ATP-ATPase; LSYN-lupeol synthase; STR-sugar transporter; ZNF-zinc finger; LY-lyase; PK-protein kinase; LCAR-L-carbamoylase; N21-nodulin 21; GDP-glycerophosphoryl diester phosphodiesterase; G3PTR-G-3-P transporter; PP-phosphatase; TDE-tumor differently expressed; SRG-senescence related gene; PEPC-phosphoenolpyruvate carboxylase; VTR-vacuolar transporter; SPI-serine protease inhibitor).
Mentions: Compared to the rhizobia-inoculated roots, acclimation to nitrate as nitrogen source leads to regulation of a limited number of genes in Lotus. Genes corresponding to only 230 IDs were found differently regulated in the nitrate-grown roots compared to untreated roots, and out of these only 90 were specific for the nitrate treatment and were not found in the pool of genes regulated in response to M. loti. These included homologs of nitrate, peptide- and phosphate-transporters that were previously found regulated in Arabidopsis in response to inorganic nitrogen (reviewed in [67]). Interestingly, nine of the genes that were regulated by inoculation with M. loti were regulated similarly in the nitrate grown roots. Among these, genes encoding an UDP-glycosyltransferase and ARR8 are found, indicating that cytokinin signalling may be important in both symbiotic and inorganic nitrogen plant nutrition (Figure 5A and Folder S7). Not surprisingly, nitrate-grown roots have more differentially expressed genes in common with the 21 dpi roots, compared to the other analyzed time points. These included genes for anthocyanidin synthase and a urea transporter, which were down-regulated, and a couple of transcriptional regulators and N21, which were up-regulated (Figure 5B).

Bottom Line: Another surprise was the extensive transcriptional response in whole root compared to the susceptible root zone where the cellular response is most pronounced.A large number of transcripts predicted to encode transcriptional regulators, receptors and proteins involved in signal transduction, as well as many genes with unknown function, were found to be regulated during nodule organogenesis and rhizobial infection.The complete data set was organized into an indexed expression directory that is accessible from a resource database, and here we present selected examples of biological questions that can be addressed with this comprehensive and powerful gene expression data set.

View Article: PubMed Central - PubMed

Affiliation: Centre for Carbohydrate Recognition and Signalling, MBI, Aarhus University, Aarhus C, Denmark.

ABSTRACT
Genetic analyses of plant symbiotic mutants has led to the identification of key genes involved in Rhizobium-legume communication as well as in development and function of nitrogen fixing root nodules. However, the impact of these genes in coordinating the transcriptional programs of nodule development has only been studied in limited and isolated studies. Here, we present an integrated genome-wide analysis of transcriptome landscapes in Lotus japonicus wild-type and symbiotic mutant plants. Encompassing five different organs, five stages of the sequentially developed determinate Lotus root nodules, and eight mutants impaired at different stages of the symbiotic interaction, our data set integrates an unprecedented combination of organ- or tissue-specific profiles with mutant transcript profiles. In total, 38 different conditions sampled under the same well-defined growth regimes were included. This comprehensive analysis unravelled new and unexpected patterns of transcriptional regulation during symbiosis and organ development. Contrary to expectations, none of the previously characterized nodulins were among the 37 genes specifically expressed in nodules. Another surprise was the extensive transcriptional response in whole root compared to the susceptible root zone where the cellular response is most pronounced. A large number of transcripts predicted to encode transcriptional regulators, receptors and proteins involved in signal transduction, as well as many genes with unknown function, were found to be regulated during nodule organogenesis and rhizobial infection. Combining wild type and mutant profiles of these transcripts demonstrates the activation of a complex genetic program that delineates symbiotic nitrogen fixation. The complete data set was organized into an indexed expression directory that is accessible from a resource database, and here we present selected examples of biological questions that can be addressed with this comprehensive and powerful gene expression data set.

Show MeSH
Related in: MedlinePlus