Callose-regulated symplastic communication 2 coordinates symbiotic root nodule development

ROCIO GAUDIOSO-PEDRAZA; MARTINA BECK; LISA FRANCES; CAROLINA RIPODAS; KIRK PHILIP; ANDREAS NIEBEL; GILES E. D. OLDROYD; YOSELIN BENITEZ-ALFONSO; FERNANDA DE CARVALHO-NIEBEL

CURRENT BIOLOGY

CELL PRESS

Lugar: United States; Año: 2018

0960-9822

The formation of nitrogen-fixing nodules in legumes involves the initiation of nodule organogenesis in the root cortex, which is tightly synchronized with symbiotic rhizobial infection in the epidermis. In this study, we provide evidence that symplastic communication, regulated by callose turnover at plasmodesmata (PD), is important for coordinating nodule development and infection in Medicago truncatula. Here we show that rhizobia induce the expression of a novel PD-associated callose-degrading enzyme, the M. truncatula β-1,3-glucanase 2 (MtBG2), in inner root tissues where nodule initiates, and where coincidently callose levels are reduced upon rhizobial inoculation. Spatiotemporal analyses revealed that MtBG2 expression expands from dividing nodule initials to rhizobia colonized cortical and epidermal tissues. As shown by the transport of fluorescent molecules in vivo, symplastic-connected domains are created in these rhizobia-colonized tissues. MtBG2 localizes to presumed PD sites and regulates symplastic flux and nodule development when constitutively expressed in roots. These findings suggest that progressive degradation of PD-callose, driven in part by the upregulation of MtBG2, creates symplastic domains during sequential nodule developmental stages.Interfering with symplastic connectivity led to drastic nodulation phenotypes. Indeed, modifying it by a MtBG2 RNAi approach, or by the controlled expression of PD-localized β-1,3-glucanases (including MtBG2) or a hyperactive callose synthase under different symbiotic promoters affected nodule development and colonization. Obstructing symplastic connectivity appears to block a signalingpathway required for the expression of Nodule Inception (NIN) and its target Nuclear Factor Y (NF-YA1) in the middle/inner cortex, while epidermal/outer cortex NIN/NF-YA1 expression is maintained. We conclude that symplastic communication between cells is proactively enhanced by rhizobia and thisis necessary to allow appropriate coordination of bacterial infection and nodule development.