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1. Functional genetic studies of symbiotic genes in Medicago truncatula indicate a role for a CCAAT-box transcription factor in rhizobial infection

Author

Cousins, Donna Rose

Subjects
579.5
Abstract

Legumes form mutualistic associations with nitrogen-fixing bacteria and arbuscular mycorrhizal (AM) fungi which increases nutrient availability to the plant. Nodulation is generally restricted to legumes and has co-opted genes required for the AM symbiosis. As a result, both associations share common genes and have analogous infection strategies, including the early lipochitooligosaccharide (LCO) signals that plants perceive from the symbionts. In order to discover novel genes required for both these symbioses, I used both forward and reverse genetic approaches. A forward genetic screen in Medicago truncatula revealed an H+-ATPase mutant Mtha1 with a defective arbuscule phenotype. The reverse screen investigated several candidates previously identified as having enhanced expression in the nodule inception mutant during nodulation that were also expressed in AM-colonized roots. Four of these genes were chosen for further study. The first, a novel AM-specific gene, BiFunctional Protein (BFP) has a predicted a role in lipid modification. Phylogenetic analysis revealed that BFP was restricted to AM host plants including a member of the liverworts, Marchantia paleacea. BFP expression during AM interactions in M. truncatula was found to be dependent on the common symbiotic gene DOES NOT MAKE INFECTIONS 3. AM colonization assays using mutants for BFP in M. truncatula and Oryza sativa were inconclusive. Three CCAAT-Binding Factor transcription factors were also studied (CBF1, CBF2 and CBF3). Promoter-reporter studies revealed that these genes are also expressed during rhizobial infection of wild type plants. While the M. truncatula cbf1 mutant did not exhibit a consistent nodulation phenotype, mutant analysis for CBF3, showed it is required for normal infection during root hair colonisation of rhizobia in M. truncatula. Based on these results and a further analysis of expression data and published work, I propose a model in which CBF3 forms a complex with NF-YA1 and NF-YC2 during early responses to LCOs during nodulation.

Published
2016

7. Three Common Symbiotic ABC Subfamily B Transporters in Medicago truncatula Are Regulated by a NIN-Independent Branch of the Symbiosis Signaling Pathway

Author

Roy, Sonali, primary, Breakspear, Andrew, additional, Cousins, Donna, additional, Torres-Jerez, Ivone, additional, Jackson, Kirsty, additional, Kumar, Anil, additional, Su, Yangyang, additional, Liu, Cheng-Wu, additional, Krom, Nick, additional, Udvardi, Michael, additional, Xu, Ping, additional, and Murray, Jeremy D., additional

Published
2021
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9. MtLAX2, a Functional Homologue of the Arabidopsis Auxin Influx Transporter AUX1, Is Required for Nodule Organogenesis1[CC-BY]

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Subjects
Indoleacetic Acids, fungi, food and beverages, Membrane Transport Proteins, Biological Transport, Articles, biochemical phenomena, metabolism, and nutrition, Plants, Genetically Modified, Plant Root Nodulation, Plant Roots, Gravitropism, Gene Expression Regulation, Plant, Medicago truncatula, Mutation, Root Nodules, Plant, Symbiosis, Plant Proteins, Rhizobium
Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of

Published
2017

11. Identification of a core set of rhizobial infection genes using data from single cell-types.

Author

Da-Song Chen, Cheng-Wu Liu, Roy, Sonali, Cousins, Donna, Stacey, Nicola, and Murray, Jeremy D.

Subjects
RHIZOBIUM, MEDICARPINS, NITROBLUE tetrazolium
Abstract

Genome-wide expression studies on nodulation have varied in their scale from entire root systems to dissected nodules or root sections containing nodule primordia (NP). More recently efforts have focused on developing methods for isolation of root hairs from infected plants and the application of laser-capture microdissection technology to nodules. Here we analyze two published data sets to identify a core set of infection genes that are expressed in the nodule and in root hairs during infection. Among the genes identified were those encoding phenylpropanoid biosynthesis enzymes including Chalcone-O-Methyltransferase which is required for the production of the potent Nod gene inducer 4',4-dihydroxy-2-methoxychalcone. A promoter-GUS analysis in transgenic hairy roots for two genes encoding Chalcone-O-Methyltransferase isoforms revealed their expression in rhizobially infected root hairs and the nodule infection zone but not in the nitrogen fixation zone. We also describe a group of Rhizobially Induced Peroxidases whose expression overlaps with the production of superoxide in rhizobially infected root hairs and in nodules and roots. Finally, we identify a cohort of co-regulated transcription factors as candidate regulators of these processes. [ABSTRACT FROM AUTHOR]

Published
2015
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12. H+-ATPase That Energizes Nutrient Uptake during Mycorrhizal Symbioses in Rice and Medicago truncatula.

Author

Wang, Ertao, Yu, Nan, Bano, S. Asma, Liu, Chengwu, Miller, Anthony J., Cousins, Donna, Zhang, Xiaowei, Ratet, Pascal, Tadege, Million, Mysore, Kirankumar S., Downie, J. Allan, Murray, Jeremy D., Oldroyd, Giles E.D., and Schultze, Michael

Subjects
MEDICAGO truncatula, MEDICAGO, PLANT membranes, SYMBIOSIS, FUNGAL membranes, NUTRIENT uptake, MEMBRANE potential
Abstract

Most plant species form symbioses with arbuscular mycorrhizal (AM) fungi, which facilitate the uptake of mineral nutrients such as phosphate from the soil. Several transporters, particularly proton-coupled phosphate transporters, have been identified on both the plant and fungal membranes and contribute to delivering phosphate from fungi to plants. The mechanism of nutrient exchange has been studied in plants during mycorrhizal colonization, but the source of the electrochemical proton gradient that drives nutrient exchange is not known. Here, we show that plasma membrane H+-ATPases that are specifically induced in arbuscule-containing cells are required for enhanced proton pumping activity in membrane vesicles from AM -colonized roots of rice (Oryza sativa) and Medicago truncatula. Mutation of the H+-ATPases reduced arbuscule size and impaired nutrient uptake by the host plant through the mycorrhizal symbiosis. Overexpression of the H+-ATPase Os-HA1 increased both phosphate uptake and the plasma membrane potential, suggesting that this H+-ATPase plays a key role in energizing the periarbuscular membrane, thereby facilitating nutrient exchange in arbusculated plant cells. [ABSTRACT FROM AUTHOR]

Published
2014
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13. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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14. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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15. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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16. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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17. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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