Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae)

Seedlings of the sweet fern, Comptonia peregrina (L.) Coult., grown aeroponically, were inoculated with a nodule suspension to allow infection by the actinomycete-like organism which causes nodule formation. Roots with early stages of infection and nodule initiation were fixed, embedded in resin, sectioned, and examined. Infection is infrequent in Comptonia with only a few nodules per seedling root system. Infection via root hair invasion causes the retention of the curled and deformed root hair in an intensely cytoplasmic state with ramification of multiple filamentous strands of the endophyte. A limited cortical proliferation occurs in response to the infection forming the prenodule; endophyte filaments grow radially inward from the base of the infected epidermal root hair and invade a portion of the prenodular cells resulting in their hypertrophy. Distal and proximal to the prenodule site, a number of primary nodule primordia are initiated, varying from a few up to a dozen or more. These primordia appear to develop more or less simultaneously under the stimulus of the invading endophyte; they are like lateral roots in their site of origin, occurring largely opposite the protoxylem poles and involving pericyclic and endodermal cell proliferation. They differ in that the cortical cells external to each primordium are stimulated to undergo divisions and these cortical cell derivatives are incorporated into the developing primordium. The endophyte enters the cortical tissues of the lateral root on which the prenodule has formed and then invades proximal and distal to the infection site, progressing into the cortical tissues of each of the developing nodule primordia. A cork-like layer develops on the original lateral root in areas not occupied by primordia by initiation of subepidermal cell divisions and wall thickening. Normal lateral root primordium formation occurs in the pericycle opposite the protoxylem poles and involves cellular derivatives of the pericycle and endodermis but no cortical cells, which instead are crushed and displaced by the lateral root primordium as it develops. Nodule formation clearly involves complex chemical interactions, which remain for further study, between the host cells and the invading endophyte.

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Effects of a Nod-factor-overproducing strain of Sinorhizobium meliloti on the expression of the ENOD40 gene in Melilotus alba

Canadian Journal of Botany ◽

10.1139/b02-076 ◽

2002 ◽

Vol 80 (9) ◽

pp. 907-915 ◽

Cited By ~ 6

Author(s):

Walter F Giordano ◽

Michelle R Lum ◽

Ann M Hirsch

Keyword(s):

Lateral Root ◽

Sinorhizobium Meliloti ◽

Cortical Cell ◽

Host Cells ◽

Nodule Development ◽

Nodule Formation ◽

Additional Increase ◽

Nod Factor ◽

Melilotus Alba ◽

Different Strains

We have initiated studies on the molecular biology and genetics of white sweetclover (Melilotus alba Desr.) and its responses to inoculation with the nitrogen-fixing symbiont Sinorhizobium meliloti. Early nodulin genes such as ENOD40 serve as markers for the transition from root to nodule development even before visible stages of nodule formation are evident. Using Northern blot analysis, we found that the ENOD40 gene was expressed within 6 h after inoculation with two different strains of S. meliloti, one of which overproduces symbiotic Nod factors. Inoculation with this strain resulted in an additional increase in ENOD40 gene expression over a typical wild-type S. meliloti strain. Moreover, the increase in mRNA brought about by the Nod-factor-overproducing strain 24 h after inoculation was correlated with lateral root formation by using whole-mount in situ hybridization to localize ENOD40 transcripts in lateral root meristems and by counting lateral root initiation sites. Cortical cell divisions were not detected. We also found that nodulation occurred more rapidly on white sweetclover in response to the Nod-factor-overproducing strain, but ultimately there was no difference in nodulation efficiency in terms of nodule number or the number of roots nodulated by the two strains. Also, the two strains could effectively co-colonize the host when inoculated together, although a few host cells were occupied by both strains.Key words: ENOD40, Nod factor, Melilotus, Sinorhizobium, symbiosis.

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Auxin: at the root of nodule development?

Functional Plant Biology ◽

10.1071/fp08177 ◽

2008 ◽

Vol 35 (8) ◽

pp. 651 ◽

Cited By ~ 87

Author(s):

Ulrike Mathesius

Keyword(s):

Lateral Root ◽

De Novo ◽

Root Nodules ◽

Lateral Roots ◽

Nodule Development ◽

Nodule Formation ◽

Cortical Cells ◽

Lateral Root Development ◽

Organ Differentiation ◽

Development And Differentiation

Root nodules are formed as a result of an orchestrated exchange of chemical signals between symbiotic nitrogen fixing bacteria and certain plants. In plants that form nodules in symbiosis with actinorhizal bacteria, nodules are derived from lateral roots. In most legumes, nodules are formed de novo from pericycle and cortical cells that are re-stimulated for division and differentiation by rhizobia. The ability of plants to nodulate has only evolved recently and it has, therefore, been suggested that nodule development is likely to have co-opted existing mechanisms for development and differentiation from lateral root formation. Auxin is an important regulator of cell division and differentiation, and changes in auxin accumulation and transport are essential for lateral root development. There is growing evidence that rhizobia alter the root auxin balance as a prerequisite for nodule formation, and that nodule numbers are regulated by shoot-to-root auxin transport. Whereas auxin requirements appear to be similar for lateral root and nodule primordium activation and organ differentiation, the major difference between the two developmental programs lies in the specification of founder cells. It is suggested that differing ratios of auxin and cytokinin are likely to specify the precursors of the different root organs.

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Lateral root initiation in Marsilea quadrifolia. I. Origin and histogenesis of lateral roots

Canadian Journal of Botany ◽

10.1139/b91-018 ◽

1991 ◽

Vol 69 (1) ◽

pp. 123-135 ◽

Cited By ~ 14

Author(s):

Bai-Ling Lin ◽

V. Raghavan

Keyword(s):

Lateral Root ◽

Single Cells ◽

Lateral Roots ◽

Central Axis ◽

Root Initiation ◽

Vascular Connection ◽

Lateral Root Initiation ◽

Marsilea Quadrifolia ◽

Lateral Root Primordium ◽

Root Primordium

In Marsilea quadrifolia, lateral roots arise from modified single cells of the endodermis located opposite the protoxylem poles within the meristematic region of the parent root. The initial cell divides in four specific planes to establish a fivecelled lateral root primordium, with a tetrahedral apical cell in the centre and the oldest merophytes and the root cap along the sides. The cells of the merophyte divide in a precise pattern to give rise to the cells of the cortex, endodermis, pericycle, and vascular tissues of the emerging lateral root. Although the construction of the parent root is more complicated than that of lateral roots, patterns of cell division and tissue formation are similar in both types of roots, with the various tissues being arranged in similar positions in relation to the central axis. Vascular connection between the lateral root primordium and the parent root is derived from the pericycle cells lying between the former and the protoxylem members of the latter. It is proposed that the central axis of the root is not only a geometric centre, but also a physiological centre which determines the fate of the different cell types. Key words: lateral root initiation, Marsilea quadrifolia, root histogenesis.

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Determinate development of nodule roots in actinomycete-induced root nodules of Myrica gale

Canadian Journal of Botany ◽

10.1139/b78-155 ◽

1978 ◽

Vol 56 (11) ◽

pp. 1357-1364 ◽

Cited By ~ 16

Author(s):

John G. Torrey ◽

Dale Callaham

Keyword(s):

Root Development ◽

Root Nodules ◽

Cortical Cell ◽

Gas Diffusion ◽

Nodule Development ◽

Nodule Formation ◽

Low Oxygen ◽

Cortical Cells ◽

Continuous Growth ◽

Myrica Gale

Young seedlings of Myrica gale L. grown in water culture were inoculated with a nodule suspension containing the effective actinomycete which induced root nodule formation. Nodule development was followed from initiation to nodule lobe formation and nodule root development using living materials and fixed nodules sectioned for light microscopy. After root hair infection and prenodule formation, three stages were observed: nodule lobe formation, a transition or arrested state, and nodule root development. The primary nodule lobe meristem originates endogenously and its formation involves pericycle, endodermis, and cortical cell derivatives. The lobe develops slowly to about 2 mm in length while the cortical cells are invaded by the actinomycete endophyte. After a period of arrest of variable duration, from a few days to several weeks, the nodule lobe meristem begins altered development, forming the elongate nodule root which undergoes slow but continuous growth to about 3- to 4-cm final length. New nodule lobe primordia are initiated endogenously at the base of existing nodules lobes, ultimately forming a cluster of nodule roots. Each nodule root, which elongates at about 0.1–1.0 mm per day, has a terminal apical meristem with reduced root cap formation and produces a modified root structure possessing an elaborate cortical intercellular space system and a reduced central cylinder. Nodule root growth is distinctive in that it shows strong negative geotropism. The endophyte is restricted to cortical cells of the nodule lobe and is totally absent from tissues of the nodule root. A probable role for nodule roots is to facilitate gas diffusion to the nitrogen-fixing endophyte site in the nodule lobe when nodules occur under conditions of low oxygen tension.

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Auxin Response Factor 2 (ARF2), ARF3, and ARF4 Mediate Both Lateral Root and Nitrogen Fixing Nodule Development in Medicago truncatula

Frontiers in Plant Science ◽

10.3389/fpls.2021.659061 ◽

2021 ◽

Vol 12 ◽

Author(s):

Cristina Kirolinko ◽

Karen Hobecker ◽

Jiangqi Wen ◽

Kirankumar S. Mysore ◽

Andreas Niebel ◽

...

Keyword(s):

Medicago Truncatula ◽

Root Development ◽

Lateral Root ◽

Lateral Roots ◽

Nodule Development ◽

Nodule Formation ◽

Mrna Levels ◽

Nitrogen Fixing ◽

Auxin Response ◽

Small Interference Rna

Auxin Response Factors (ARFs) constitute a large family of transcription factors that mediate auxin-regulated developmental programs in plants. ARF2, ARF3, and ARF4 are post-transcriptionally regulated by the microRNA390 (miR390)/trans-acting small interference RNA 3 (TAS3) module through the action of TAS3-derived trans-acting small interfering RNAs (ta-siRNA). We have previously reported that constitutive activation of the miR390/TAS3 pathway promotes elongation of lateral roots but impairs nodule organogenesis and infection by rhizobia during the nitrogen-fixing symbiosis established between Medicago truncatula and its partner Sinorhizobium meliloti. However, the involvement of the targets of the miR390/TAS3 pathway, i.e., MtARF2, MtARF3, MtARF4a, and MtARF4b, in root development and establishment of the nitrogen-fixing symbiosis remained unexplored. Here, promoter:reporter fusions showed that expression of both MtARF3 and MtARF4a was associated with lateral root development; however, only the MtARF4a promoter was active in developing nodules. In addition, up-regulation of MtARF2, MtARF3, and MtARF4a/b in response to rhizobia depends on Nod Factor perception. We provide evidence that simultaneous knockdown of MtARF2, MtARF3, MtARF4a, and MtARF4b or mutation in MtARF4a impaired nodule formation, and reduced initiation and progression of infection events. Silencing of MtARF2, MtARF3, MtARF4a, and MtARF4b altered mRNA levels of the early nodulation gene nodulation signaling pathway 2 (MtNSP2). In addition, roots with reduced levels of MtARF2, MtARF3, MtARF4a, and MtARF4b, as well as arf4a mutant plants exhibited altered root architecture, causing a reduction in primary and lateral root length, but increasing lateral root density. Taken together, our results suggest that these ARF members are common key players of the morphogenetic programs that control root development and the formation of nitrogen-fixing nodules.

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Lateral root development in a woody plant, Quercus suber L. (cork oak)

Canadian Journal of Botany ◽

10.1139/b00-077 ◽

2000 ◽

Vol 78 (9) ◽

pp. 1125-1135

Author(s):

Dolors Verdaguer ◽

Pedro J Casero ◽

Marisa Molinas

Keyword(s):

Root Development ◽

Lateral Root ◽

Root Meristem ◽

Lateral Roots ◽

Quercus Suber ◽

Cork Oak ◽

Vascular Connection ◽

Lateral Root Development ◽

Lateral Root Primordium ◽

Root Primordium

The distribution and the ontogenesis of lateral roots have been investigated in the Mediterranean woody species Quercus suber L. (cork oak). Lateral roots arose in protoxylem-based ranks and a tendency to clumping was observed. Three stages are distinguished in lateral root primordium development. Lateral root primordia are derived mainly from pericycle cells. The endodermis contributed to the initial lateral root development, forming an endodermal cover that sloughs off with lateral root emergence. The unemerged lateral roots show an incipient layered root meristem; this meristem can be classified as a closed type meristem. Primary vascular connection takes place with the xylem strand opposite the lateral root primordium and the two adjacent phloem strands. Primary vascular connector elements are derived from pericyclic derivative cells. Vascular parenchyma cells contribute mainly in the development of the cambium and the subsequent secondary xylem and phloem connector elements. The secondary vascular elements of the lateral root and parent root differentiate in continuity. Vascular connection is discussed in relation to the root vascular plexus described in monocotyledonous and in some herbaceous dicotyledonous plants. An endodermis with suberized lamellae is continuous between the lateral and parent root in emerged lateral roots.Key words: lateral root, development pattern, apical lateral root meristem, root vascular connection, Quercus suber L.

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Cortical Cell Breakdown and Lateral Root Primordium Development inVicia fabaL

Journal of Experimental Botany ◽

10.1093/jxb/27.5.922 ◽

1976 ◽

Vol 27 (5) ◽

pp. 922-932 ◽

Cited By ~ 8

Author(s):

R. D. MACLEOD ◽

D. FRANCIS

Keyword(s):

Lateral Root ◽

Cortical Cell ◽

Lateral Root Primordium ◽

Root Primordium ◽

Cell Breakdown

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The Auxin-Regulated AP2/EREBP Gene PUCHI Is Required for Morphogenesis in the Early Lateral Root Primordium of Arabidopsis

The Plant Cell ◽

10.1105/tpc.107.050674 ◽

2007 ◽

Vol 19 (7) ◽

pp. 2156-2168 ◽

Cited By ~ 103

Author(s):

Atsuko Hirota ◽

Takehide Kato ◽

Hidehiro Fukaki ◽

Mitsuhiro Aida ◽

Masao Tasaka

Keyword(s):

Lateral Root ◽

Lateral Root Primordium ◽

Root Primordium

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Identification of Symbiotically Defective Mutants of Lotus japonicus Affected in Infection Thread Growth

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-19-1444 ◽

2006 ◽

Vol 19 (12) ◽

pp. 1444-1450 ◽

Cited By ~ 20

Author(s):

Fabien Lombardo ◽

Anne B. Heckmann ◽

Hiroki Miwa ◽

Jillian A. Perry ◽

Koji Yano ◽

...

Keyword(s):

Root Hair ◽

Plant Cell Wall ◽

Plant Root ◽

Lotus Japonicus ◽

Cortical Cell ◽

Host Cells ◽

Infection Thread ◽

Mycorrhizal Symbiosis ◽

Symbiotic Interaction ◽

Infection Threads

During the symbiotic interaction between legumes and rhizobia, the host cell plasma membrane and associated plant cell wall invaginate to form a tunnel-like infection thread, a structure in which bacteria divide to reach the plant root cortex. We isolated four Lotus japonicus mutants that make infection pockets in root hairs but form very few infection threads after inoculation with Mesorhizobium loti. The few infection threads that did initiate in the mutants usually did not progress further than the root hair cell. These infection-thread deficient (itd) mutants were unaffected for early symbiotic responses such as calcium spiking, root hair deformation, and curling, as well as for the induction of cortical cell division and the arbuscular mycorrhizal symbiosis. Complementation tests and genetic mapping indicate that itd2 is allelic to Ljsym7, whereas the itd1, itd3, and itd4 mutations identified novel loci. Bacterial release into host cells did occur occasionally in the itd1, itd2, and itd3 mutants suggesting that some infections may succeed after a long period and that infection of nodule cells could occur normally if the few abnormal infection threads that were formed reached the appropriate nodule cells.

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