Getting around the legume nodule: II. Molecular biology of its peripheral zone and approaches to study its vasculature

Abstract

All legume nodules exhibit a complex cortex composed of many types of cells and tissues. This zone, which surrounds the central infected zone, plays a critical role in regulating the exchange of oxygen between the rhizosphere and the bacteroids. Not often mentioned, but of importance, are the vascular traces that develop in the nodule inner cortex. Information on their ontogeny is scarce, although their existence is critical to the symbiosis because both the nitrogenous compounds formed as a result of nitrogenase activity and the energy-rich molecules obtained from plant photosynthesis use these conduits. Here, I focus on these tissues, reviewing what we know of their appearance in pseudonodules, borontreated legumes, and in the vasculature mutants described to date. I also examine the genes known to be expressed in the peripheral tissues and attempt to place them in functional clusters. Finally, I propose that specific vasculature markers known from the Arabidopsis literature be applied to the study of the development of nodule vascular tissues. It is of interest that most of these markers are linked to specific growth regulators, especially auxins and cytokinins but to a lesser extent gibberellins and brassinosteroids.Résumé : Toutes les nodosités se développant sur les racines de légumineuses ont un cortex composé de nombreux tissus. Cette zone, qui entoure la zone centrale infectée par les bactéries, joue un rôle essentiel dans la régulation de l'oxygène échangé entre la rhizosphère et les bactéroïdes. De plus, elle est importante, car dans sa partie interne on y trouve les traces vasculaires responsables du transport des composés azotés produits par l'activité de la nitrogénase et de celui des molécules riches en énergie résultant de la photosynthèse. Bien que ces tissus conducteurs soient indispensables au fonctionnement du nodule, on ne sait que peu de choses sur leur ontogénie. Dans cette synthèse, l'intérêt est porté sur ces tissus; je rends compte de ce que l'on connaît sur leur apparence dans les pseudo-nodosités, dans les nodules qui se forment chez les légumineuses traitées avec du bore, et dans ceux se développant chez les mutants de légumineuses exhibant des défauts dans leurs tissus vasculaires. De plus, j'ai groupé par clusters fonctionnels les gènes connus pour s'exprimer dans les tissus périphériques de la nodosité. Enfin, je propose que l'usage de gènes marqueurs spécifiques pour les tissus conducteurs chez Arabidopsis soi étendu à l'étude du développement des tissus vasculaires du nodule. Il est intéressant de noter que la plupart des marqueurs mentionnés dans cette synthèse soient liés à des régulateurs de croissance, tels que l'auxine et la cytokinine mais aussi la gibbérelline et la brassinostéroïde.Mots-clés : bore, mutant affecté dans leur nodulation, nodule de type desmodioïde, nodule de type indéterminé, nodule spontané, régulateur de croissance, tissus vasculaires.

The SNARE Protein SYP71 Expressed in Vascular Tissues Is Involved in Symbiotic Nitrogen Fixation in Lotus japonicus Nodules

“…The nitrogen-fixing activity of the nodules could be impaired by an interruption in the translocation of either substance, which is caused by the LjSYP71 mutation. Guinel (2009) focused on the legume nodule cortex surrounding the central infected zone and highlighted the importance of vascular tissues in the development and regulation of nodules in the legume-rhizobium symbiosis. Our results present further evidence for the pivotal role played by the vasculature in symbiotic nitrogen fixation.…”

Ethylene, a Hormone at the Center-Stage of Nodulation

“…The correct expression of the genes comprised in the CSTP ( Figure 1 , green box) is required for nodulation success and if one of these genes is mutated, the nodulation process aborts ( Oldroyd, 2013 ). It is possible for the two nodulation programs to be uncoupled since pseudo-nodules can form in the absence of bacteria; in such cases, the cortical program is activated on its own, independently of the epidermal program (for a review, see Guinel, 2009b ). Such nodules form spontaneously on Lotus japonicus roots when the CCaMK/SNF1 gene, coding for a calcium- and calmodulin-dependent kinase, is mutated ( Gleason et al, 2006 ; Tirichine et al, 2006a ) or when a phosphomimetic version of the CYCLOPS gene, coding for a phosphorylation substrate of CCaMK, is used ( Singh et al, 2014 ).…”

Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types

“…It would be interesting to test whether or not differential hormone sensitivity of individual pericycle cells explains the difference observed in the numbers of nodules facing xylem and phloem. It is well known that nodule initiation is tightly coupled with the induction of certain hormones (e.g., Heidstra et al 1997;Mathesius et al 1998) and it would be fruitful to study the very early stages of nodule vasculature formation using molecular markers known to play a role in vasculature differentiation, as de Billy et al (2001) have already done in M. truncatula with the LAX gene (Guinel 2009). Such a study complemented with the use of markers known to be responsive to hormones (e.g., auxin-responsive reporter constructs, Mathesius et al 1998) could help determine if the heterogeneity of the pericycle is translated in the vasculature of the nodule.…”