Summary• The infection of white lupin ( Lupinus albus ) roots and the early stages in organogenesis of the lupinoid nodule are characterized in detail in this work.• Immunolabelling of Bradyrhizobium sp. ( Lupinus ) ISLU16 and green fluorescent protein labelling of Mesorhizobium loti NZP2037, two strains that induce nodulation in L. albus , allowed us to monitor the infection and morphogenesis process. Light and transmission electron microscopy, low-temperature scanning electron microscopy, fluorescence and confocal microscopy were employed.• Rhizobia penetrated the root intercellularly at the junction between the root hair base and an adjacent epidermal cell. Bacteria invaded the subepidermal cortical cell immediately beneath the root hair through structurally altered cell wall regions. The newly infected cell divided repeatedly to form the central infected zone of the young nodule. Bacteria seemed to be equally distributed between the daughter cells.• A new mode of direct epidermal infection and an unusual morphogenesis for indeterminate nodules lead to the formation of the lupinoid nodule with unique characteristics.
Lotus japonicus determinate nodules differ greatly from indeterminate nodules in their organogenesis and morphological characteristics, whereas Lupinus albus lupinoid nodules share features of determinate and indeterminate nodules. The mitotic inhibitor Ccs52A is essential for endoreduplication and ploidy-dependent cell enlargement during symbiotic cell differentiation in Medicago truncatula indeterminate nodules. ccs52A homolog genes were isolated from lupin and lotus nodules; the deduced Ccs52A proteins showed high sequence similarity with other Cdh-1-type activators of the anaphase-promoting complex and were grouped with A-type Ccs52 proteins from different plants. In lupin, ccs52A expression was restricted to the earlier stages of nodule development, whereas ccs52A transcripts accumulated in lotus nodule primordia and, to a lesser extent, in mature nodules. Nodule development in Lupinus albus involved a progressive increase in nuclear and cellular size and ploidy level; similarly, Lotus japonicus nodules contained polyploid nuclei and enlarged cells in the infected zone. Nevertheless, in situ hybridization experiments showed the highest ccs52A expression in the inner cortex cells of the lupin nodule primordium, probably associated to the increased size of these cells in mature nodules. In view of our results, Ccs52A-mediated endoreduplication appears to be a universal mechanism required for nodule cell differentiation during the establishment of nitrogen-fixing symbioses.
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