Abstract
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 nodule organogenesis involves degradation of callose and the induced expression of a novel PD-associated callose-degrading enzyme (MtBG2) in inner root tissues where nodule initiates. MtBG2 is PD-localized and reduces PDcallose levels when constitutively expressed in roots. Spatio-temporal analyses revealed that MtBG2 expression expands from dividing nodule initials to rhizobial-colonized cortical and epidermal tissues. As shown by the transport of fluorescent molecules in vivo, symplastic-connected domains are created in these rhizobial-colonized tissues. These findings highlight 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 in rhizobial-infected tissues led to drastic nodulation phenotypes. Indeed, enhancing or blocking it by the controlled expression of PD-localized β- 1,3-glucanases (including MtBG2) or a hyperactive callose synthase, led to enhanced or reduced numbers of colonized nodules respectively. Obstructing symplastic connectivity appears to block the transmission of a diffusible signal required for the expression of Nodule Inception (NIN) in the cortex, while epidermal NIN expression is maintained. We conclude that symplastic communication between cells is proactively enhanced by rhizobia and this is necessary to allow appropriate coordination of bacterial infection and nodule development.
Highlights
Legumes establish symbiotic associations with nitrogen-fixing rhizobia, which, hosted within newly formed root nodules, have the optimized environment for fixing atmospheric dinitrogen for the plant [1]
We show that callose is reduced in root tissues forming the primordia and that this correlates with the progressive expression of a rhizobia-induced, PD-located, callose-degrading enzyme
Rhizobial Inoculation Modulates Callose Levels and the Early Expression of Callose-Degrading b-1,3Glucanases in M. truncatula Roots Past research indicates that symplastic connectivity increases between phloem and nodule initials as early as 48 hr upon inoculation with rhizobia [34], raising the question of whether callose regulation is involved in this process
Summary
Legumes establish symbiotic associations with nitrogen-fixing rhizobia, which, hosted within newly formed root nodules, have the optimized environment for fixing atmospheric dinitrogen for the plant [1]. Endosymbiotic entry occurs via newly formed tubular structures, initiated from bacterial-entrapped root hairs, called infection threads (ITs) [2]. This host-constructed transcellular compartment guides rhizobia to the underlying nodule primordium in the cortex, where the bacteria are released and differentiate into nitrogen-fixing bacteroids. Nodule development engages local hormonal changes and is tightly controlled by a systemic autoregulatory pathway (AON) that restricts nodule number [4] Diffusible hormones, such as cytokinin and auxin [5, 6], are important for initiating nodule organogenesis, little is known of how signal transmission is regulated from the infection site to underlying root tissues to coordinate nodule development
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