A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators.
Legumes host their Rhizobium spp. symbiont in novel root organs called nodules. Nodules originate from differentiated root cortical cells that dedifferentiate and subsequently form nodule primordia, a process controlled by cytokinin. A whole-genome duplication has occurred at the root of the legume Papilionoideae subfamily. We hypothesize that gene pairs originating from this duplication event and are conserved in distinct Papilionoideae lineages have evolved symbiotic functions. A phylogenetic strategy was applied to search for such gene pairs to identify novel regulators of nodulation, using the cytokinin phosphorelay pathway as a test case. In this way, two paralogous type-A cytokinin response regulators were identified that are involved in root nodule symbiosis. Response Regulator9 (MtRR9) and MtRR11 in medicago (Medicago truncatula) and an ortholog in lotus (Lotus japonicus) are rapidly induced upon Rhizobium spp. Nod factor signaling. Constitutive expression of MtRR9 results in arrested primordia that have emerged from cortical, endodermal, and pericycle cells. In legumes, lateral root primordia are not exclusively formed from pericycle cells but also require the involvement of the root cortical cell layer. Therefore, the MtRR9-induced foci of cell divisions show a strong resemblance to lateral root primordia, suggesting an ancestral function of MtRR9 in this process. Together, these findings provide a proof of principle for the applied phylogenetic strategy to identify genes with a symbiotic function in legumes.
Department of Plant Sciences, Laboratory of Molecular Biology, Wageningen University, 6708 PB, Wageningen, The Netherlands.
Rik H M
RH
Op den Camp
Stéphane
S
De Mita
Alessandra
A
Lillo
Qingqin
Q
Cao
Erik
E
Limpens
Ton
T
Bisseling
René
R
Geurts
D001483:Base Sequence; D005075:Biological Evolution; D002455:Cell Division; D003583:Cytokinins / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D020131:Genes, Duplicate / Q000235:genetics; D017343:Genes, Plant / Q000235:genetics*; D018745:Genome, Plant / Q000235:genetics*; D000070116:Lotus / Q000235:genetics / Q000382:microbiology / Q000502:physiology; D046913:Medicago truncatula / Q000166:cytology / Q000235:genetics* / Q000382:microbiology / Q000502:physiology; D008969:Molecular Sequence Data; D010802:Phylogeny; D010937:Plant Growth Regulators / Q000378:metabolism*; D011401:Promoter Regions, Genetic; D053204:Root Nodules, Plant / Q000235:genetics; D036226:Seedlings / Q000166:cytology / Q000235:genetics / Q000382:microbiology / Q000502:physiology; D017422:Sequence Analysis, DNA; D015398:Signal Transduction; D020579:Sinorhizobium / Q000502:physiology*; D013025:Glycine max / Q000235:genetics / Q000382:microbiology / Q000502:physiology; D013559:Symbiosis / Q000502:physiology
D003583:Cytokinins; D010937:Plant Growth Regulators