Transcriptome analysis of Medicago truncatula nodules has led to the discovery of a gene family named NCR (nodule-specific cysteine rich) with more than 300 members. The encoded polypeptides were short (60-90 amino acids), carried a conserved signal peptide, and, except for a conserved cysteine motif, displayed otherwise extensive sequence divergence. Family members were found in pea (Pisum sativum), broad bean (Vicia faba), white clover (Trifolium repens), and Galega orientalis but not in other plants, including other legumes, suggesting that the family might be specific for galegoid legumes forming indeterminate nodules. Gene expression of all family members was restricted to nodules except for two, also expressed in mycorrhizal roots. NCR genes exhibited distinct temporal and spatial expression patterns in nodules and, thus, were coupled to different stages of development. The signal peptide targeted the polypeptides in the secretory pathway, as shown by green fluorescent protein fusions expressed in onion (Allium cepa) epidermal cells. Coregulation of certain NCR genes with genes coding for a potentially secreted calmodulin-like protein and for a signal peptide peptidase suggests a concerted action in nodule development. Potential functions of the NCR polypeptides in cell-to-cell signaling and creation of a defense system are discussed.Plants have evolved symbiotic associations with soil microorganisms to facilitate their mineral nutrition. An example is the specific interaction of different species of the Leguminosae (legumes) with the nitrogen-fixing soil bacteria from the Rhizobiaceae family (rhizobia). This symbiosis leads to the de novo formation of a root organ, the nodule, hosting nitrogen-fixing rhizobia that feed the host plant with ammonium. Another example is the widespread association of plants with fungi from the order of Glomales leading to the formation of arbuscular endomycorrhiza that extends the plant root system and facilitates nutrient uptake. The initial stages of rhizobial and mycorrhizal interactions share certain common molecular mechanisms (Albrecht et al., 1999;Kistner and Parniske, 2002). Because mycorrhizas are more common and ancient, the rhizobial symbiosis might have acquired existing mechanisms from them.Two major types of legume nodules are distinguished (Crespi and Gálvez, 2000): the indeterminate type, formed by e.g. Medicago truncatula, pea (Pisum sativum), broad bean (Vicia faba), white clover (Trifolium repens), or Galega orientalis, and the determinate type, formed by e.g. Lotus japonicus or soybean (Glycine max). Indeterminate nodules have a complex structure composed of different central tissues surrounded by a cortex (Vasse et al., 1990). The persistent apical meristem is zone I. In zone II, postmeristematic cells gradually differentiate and become infected with rhizobia, encapsulated in a membrane envelope. Interzone II-III is characterized by amyloplast accumulation and major transcriptional changes in both plant and bacterial cells. The proximal zone III is compos...
The legume plant Medicago truncatula establishes a symbiosis with the nitrogen-fixing bacterium Sinorhizobium meliloti which takes place in root nodules. The formation of nodules employs a complex developmental program involving organogenesis, specific cellular differentiation of the host cells and the endosymbiotic bacteria, called bacteroids, as well as the specific activation of a large number of plant genes. By using a collection of plant and bacterial mutants inducing non-functional, Fix− nodules, we studied the differentiation processes of the symbiotic partners together with the nodule transcriptome, with the aim of unravelling links between cell differentiation and transcriptome activation. Two waves of transcriptional reprogramming involving the repression and the massive induction of hundreds of genes were observed during wild-type nodule formation. The dominant features of this “nodule-specific transcriptome” were the repression of plant defense-related genes, the transient activation of cell cycle and protein synthesis genes at the early stage of nodule development and the activation of the secretory pathway along with a large number of transmembrane and secretory proteins or peptides throughout organogenesis. The fifteen plant and bacterial mutants that were analyzed fell into four major categories. Members of the first category of mutants formed non-functional nodules although they had differentiated nodule cells and bacteroids. This group passed the two transcriptome switch-points similarly to the wild type. The second category, which formed nodules in which the plant cells were differentiated and infected but the bacteroids did not differentiate, passed the first transcriptome switch but not the second one. Nodules in the third category contained infection threads but were devoid of differentiated symbiotic cells and displayed a root-like transcriptome. Nodules in the fourth category were free of bacteria, devoid of differentiated symbiotic cells and also displayed a root-like transcriptome. A correlation thus exists between the differentiation of symbiotic nodule cells and the first wave of nodule specific gene activation and between differentiation of rhizobia to bacteroids and the second transcriptome wave in nodules. The differentiation of symbiotic cells and of bacteroids may therefore constitute signals for the execution of these transcriptome-switches.
Systematic sequencing of expressed sequence tags (ESTs) can give a global picture of the assembly of genes involved in the development and function of organs. Indeterminate nodules representing different stages of the developmental program are especially suited to the study of organogenesis. With the vector lambdaHybriZAP, a cDNA library was constructed from emerging nodules of Medicago truncatula induced by Sinorhizobium meliloti. The 5' ends of 389 cDNA clones were sequenced, then these ESTs were analyzed both by sequence homology search and by studying their expression in roots and nodules. Two hundred fifty-six ESTs exhibited significant similarities to characterized data base entries and 40 of them represented 26 nodulin genes, while 133 had no similarity to sequences with known function. Only 60 out of the 389 cDNA clones corresponded to previously submitted M. truncatula EST sequences. For 117 cDNAs, reverse Northern (RNA) hybridization with root and nodule RNA probes revealed enhanced expression in the nodule, 48 clones are likely to code for novel nodulins, 33 cDNAs are clones of already known nodulin genes, and 36 clones exhibit similarity to other characterized genes. Thus, systematic analysis of the EST sequences and their expression patterns is a powerful way to identify nodule-specific and nodulation-related genes.
(M.L., P.L., P.A.)Phytohormones as well as temporal and spatial regulation of the cell cycle play a key role in plant development. Here, we investigated the function and regulation of an alfalfa (Medicago sativa) A2-type cyclin in three distinct root developmental programs: in primary and secondary root development, nodule development, and nematode-elicited gall formation. Using transgenic plants carrying the Medsa;cycA2;2 promoter--glucuronidase gene fusion, in combination with other techniques, cycA2;2 expression was localized in meristems and proliferating cells in the lateral root and nodule primordia. Rapid induction of cycA2;2 by Nod factors demonstrated that this gene is implicated in cell cycle activation of differentiated cells developing to nodule primordia. Surprisingly, cycA2;2 was repressed in the endoreduplicating, division-arrested cells both during nodule development and formation of giant cells in nematode-induced galls, indicating that CycA2;2 was dispensable for S-phase in endoreduplication cycles. Overexpression of cycA2;2 in transgenic plants corresponded to wild type protein levels and had no apparent phenotype. In contrast, antisense expression of cycA2;2 halted regeneration of somatic embryos, suggesting a role for CycA2;2 in the formation or activity of apical meristems. Expression of cycA2;2 was up-regulated by auxins, as expected from the presence of auxin response elements in the promoter. Moreover, auxin also affected the spatial expression pattern of this cyclin by shifting the cycA2;2 expression from the phloem to the xylem poles.Cyclins are the regulatory subunits of cyclindependent kinase complexes whose ordered, consecutive, and periodic activities drive the cell cycle. Cyclins are classified as G1 and mitotic cyclins. The latter group comprises the A-and B-type cyclins involved in the regulation of the cell cycle from the S to M phases. Cyclins are usually present for short periods in the cell cycle when they activate their CDK partners and determine the substrate specificity as well as the localization, maintenance and stability of these protein complexes. The activity of the cyclin-CDK complexes is tightly controlled during cell cycle and organ development.In plants, where organogenesis takes place continuously, most cells maintain their ability to re-enter and to regulate the cell cycle, in response to a wide range of external signals. The phytohormones, mostly auxin and cytokinin endogenously exert a temporal and local control on the cell cycle (Stals and Inzé, 2001). They act at multiple levels affecting transcription of cell cycle genes or the activity of the cyclin-dependent kinases; moreover, their altered balance seems to be required at specific points of the cell cycle. It is largely unknown how these external and internal signals interact and how their actions are coordinated and integrated into developmental programs.The plasticity of plant cell cycle may rely on the evolution of multiple cyclin forms. The sequence of the Arabidopsis genome indicates the existence ...
This paper presents the map and DNA sequence analysis of pRi8196 transferred DNA (T-DNA) genes encoding root-inducing and mannopine synthesis functions. A canonical 24-base-pair border repeat as well as two "pseudoborders" are present at the functional right T-DNA border. To the left of this border are homologs ofthe masi' and mas2' genes of TR pRiA4. Next to these are five open reading frames (ORFs) homologous to ORFs 1-14 of TL of pRiA4. ORFs 10-12 (roL4, roWl, and roi) are less related to their pRiA4 homologs than are the other large ORFs analyzed here. In contrast to T-DNA genes of pRiA4, pRi8196 T-DNA ORFs 11 and 12 (rolB and roiC) are sufficient to induce hairy roots on carrot disks.
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