Abstract
The number of legume root nodules resulting from a symbiosis with rhizobia is tightly controlled by the plant. Certain members of the CLAVATA3/Embryo Surrounding Region (CLE) peptide family, specifically MtCLE12 and MtCLE13 in Medicago truncatula, act in the systemic autoregulation of nodulation (AON) pathway that negatively regulates the number of nodules. Little is known about the molecular pathways that operate downstream of the AON-related CLE peptides. Here, by means of a transcriptome analysis, we show that roots ectopically expressing MtCLE13 deregulate only a limited number of genes, including three down-regulated genes encoding lysin motif receptor-like kinases (LysM-RLKs), among which are the nodulation factor (NF) receptor NF Perception gene (NFP) and two up-regulated genes, MtTML1 and MtTML2, encoding Too Much Love (TML)-related Kelch-repeat containing F-box proteins. The observed deregulation was specific for the ectopic expression of nodulation-related MtCLE genes and depended on the Super Numeric Nodules (SUNN) AON RLK. Moreover, overexpression and silencing of these two MtTML genes demonstrated that they play a role in the negative regulation of nodule numbers. Hence, the identified MtTML genes are the functional counterpart of the Lotus japonicus TML gene shown to be central in the AON pathway. Additionally, we propose that the down-regulation of a subset of LysM-RLK-encoding genes, among which is NFP, might contribute to the restriction of further nodulation once the first nodules have been formed.
Highlights
Under nitrogen-limited conditions, legume plants interact with 2013; Suzaki et al, 2015; Gamas et al, 2017)
These results suggest that in M. truncatula autoregulation of nodulation (AON)-related CLAVATA3/Embryo Surrounding Region (CLE) peptides act through the root activity of Too Much Love (TML) F-box proteins and could inhibit nodule formation via the down-regulation of genes involved in nodulation factor (NF) perception, such as NF Perception gene (NFP) and other related lysin motif (LysM)-receptor-like kinase (RLK) genes
Comparison of the proteins revealed that LjTML was 89% and 73% similar to MtTML1 and MtTML2, respectively.A similarity tree was generated with the three proteins from M. truncatula, L. japonicus, and A. thaliana most closely related to MtTML1 (Supplementary Fig S1)
Summary
Under nitrogen-limited conditions, legume plants interact with 2013; Suzaki et al, 2015; Gamas et al, 2017). Genetic analyses in L. japonicus revealed that the too much love (tml) mutant is affected in a gene acting downstream of the LjCLE–RS/LjHAR1 pathway in roots (Magori et al, 2009; Takahara et al, 2013).The LjTML gene encodes a Kelch-repeat F-box protein that is probably involved in the targeted ubiquitin-dependent proteolysis of still unknown nuclear proteins that are expected to be critical for early nodulation. We show that only a limited set of root genes were differentially regulated, including NFP and some LysM-RLK-related genes, as well as two TML orthologs Together, these results suggest that in M. truncatula AON-related CLE peptides act through the root activity of TML F-box proteins and could inhibit nodule formation via the down-regulation of genes involved in NF perception, such as NFP and other related LysM-RLK genes
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