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

2021 ◽  
Vol 12 ◽  
Author(s):  
Cristina Kirolinko ◽  
Karen Hobecker ◽  
Jiangqi Wen ◽  
Kirankumar S. Mysore ◽  
Andreas Niebel ◽  
...  

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.

2001 ◽  
Vol 14 (3) ◽  
pp. 267-277 ◽  
Author(s):  
Françoise de Billy ◽  
Cathy Grosjean ◽  
Sean May ◽  
Malcolm Bennett ◽  
Julie V. Cullimore

Medicago truncatula contains a family of at least five genes related to AUX1 of Arabidopsis thaliana (termed MtLAX genes for Medicago truncatula-like AUX1 genes). The high sequence similarity between the encoded proteins and AUX1 implies that the MtLAX genes encode auxin import carriers. The MtLAX genes are expressed in roots and other organs, suggesting that they play pleiotropic roles related to auxin uptake. In primary roots, the MtLAX genes are expressed preferentially in the root tips, particularly in the provascular bundles and root caps. During lateral root and nodule development, the genes are expressed in the primordia, particularly in cells that were probably derived from the pericycle. At slightly later stages, the genes are expressed in the regions of the developing organs where the vasculature arises (central position for lateral roots and peripheral region for nodules). These results are consistent with MtLAX being involved in local auxin transport and suggest that auxin is required at two common stages of lateral root and nodule development: development of the primordia and differentiation of the vasculature.


2008 ◽  
Vol 35 (8) ◽  
pp. 651 ◽  
Author(s):  
Ulrike Mathesius

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.


1977 ◽  
Vol 55 (17) ◽  
pp. 2306-2318 ◽  
Author(s):  
Dale Callaham ◽  
John G. Torrey

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.


2019 ◽  
Author(s):  
Feng Zhang ◽  
Wenqing Tao ◽  
Ruiqi Sun ◽  
Junxia Wang ◽  
Cuiling Li ◽  
...  

AbstractThe development of lateral roots in Arabidopsis thaliana is strongly dependent on signaling directed by the AUXIN RESPONSE FACTOR7 (ARF7), which in turn activates LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors (LBD16, 18, 29 and 33). Here, the product of PRH1, a PR-1 homolog annotated previously as encoding a pathogen-responsive protein, was identified as a target of ARF7-mediated auxin signaling and also as participating in the development of lateral roots. PRH1 was shown to be strongly induced by auxin treatment, and plants lacking a functional copy of PRH1 formed fewer lateral roots. The transcription of PRH1 was controlled by the binding of both ARF7 and LBDs to its promoter region. An interaction was detected between PRH1 and GATA23, a protein which regulates cell identity in lateral root founder cells.Author SummaryIn Arabidopsis thaliana AUXIN RESPONSE FACTOR7 (ARF7)-mediated auxin signaling plays a key role in lateral roots (LRs) development. The LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors (LBD16, 18, 29 and 33) act downstream of ARF7-mediated auxin signaling to control LRs formation. Here, the PR-1 homolog PRH1 was identified as a novel target of both ARF7 and LBDs (especially the LBD29) during auxin induced LRs formation, as both ARF7 and LBDs were able to bind to the PRH1 promoter. More interestingly, PRH1 has a physical interaction with GATA23, which has been also reported to be up-regulated by auxin and influences LR formation through its regulation of LR founder cell identity. Whether the interaction between GATA23 and PRH1 affects the stability and/or the activity of either (or both) of these proteins remains an issue to be explored. This study provides improves new insights about how auxin regulates lateral root development.


2005 ◽  
Vol 18 (6) ◽  
pp. 521-532 ◽  
Author(s):  
Lydia J. Bright ◽  
Yan Liang ◽  
David M. Mitchell ◽  
Jeanne M. Harris

The evolutionary origins of legume root nodules are largely unknown. We have identified a gene,LATD, of the model legume Medicago truncatula, that is required for both nodule and root development, suggesting that these two developmental processes may share a common evolutionary origin. The latd mutant plants initiate nodule formation but do not complete it, resulting in immature, non-nitrogen-fixing nodules. Similarly, lateral roots initiate, but remain shortstumps. The primary root, which initially appears to be wild type, gradually ceases growth and forms an abnormal tipthat resembles that of the mutant lateral roots. Infection by the rhizobial partner, Sinorhizobium meliloti, can occur, although infection is rarely completed. Once inside latd mutant nodules, S. meliloti fails to express rhizobial genes associatedwith the developmental transition from free-living bacterium to endosymbiont, such as bacA and nex38. The infecting rhizobia also fail to express nifH and fix nitrogen. Thus, both plant and bacterial development are blocked in latd mutant roots. Based on the latd mutant phenotype, we propose that the wild-type function of the LATD gene is to maintain root meristems. The strong requirement of both nodules and lateral roots for wild-type LATD gene function supports lateral roots as a possible evolutionary origin for legume nodules.


2019 ◽  
Vol 19 (1) ◽  
Author(s):  
Defeng Shen ◽  
Olga Kulikova ◽  
Kerstin Guhl ◽  
Henk Franssen ◽  
Wouter Kohlen ◽  
...  

Abstract Background Legumes can utilize atmospheric nitrogen by hosting nitrogen-fixing bacteria in special lateral root organs, called nodules. Legume nodules have a unique ontology, despite similarities in the gene networks controlling nodule and lateral root development. It has been shown that Medicago truncatula NODULE ROOT1 (MtNOOT1) is required for the maintenance of nodule identity, preventing the conversion to lateral root development. MtNOOT1 and its orthologs in other plant species -collectively called the NOOT-BOP-COCH-LIKE (NBCL) family- specify boundary formation in various aerial organs. However, MtNOOT1 is not only expressed in nodules and aerial organs, but also in developing roots, where its function remains elusive. Results We show that Mtnoot1 mutant seedlings display accelerated root elongation due to an enlarged root apical meristem. Also, Mtnoot1 mutant roots are thinner than wild-type and are delayed in xylem cell differentiation. We provide molecular evidence that the affected spatial development of Mtnoot1 mutant roots correlates with delayed induction of genes involved in xylem cell differentiation. This coincides with a basipetal shift of the root zone that is susceptible to rhizobium-secreted symbiotic signal molecules. Conclusions Our data show that MtNOOT1 regulates the size of the root apical meristem and vascular differentiation. Our data demonstrate that MtNOOT1 not only functions as a homeotic gene in nodule development but also coordinates the spatial development of the root.


2019 ◽  
Vol 71 (4) ◽  
pp. 1562-1573 ◽  
Author(s):  
Jason L P Ng ◽  
Astrid Welvaert ◽  
Jiangqi Wen ◽  
Rujin Chen ◽  
Ulrike Mathesius

Abstract The development of root nodules leads to an increased auxin response in early nodule primordia, which is mediated by changes in acropetal auxin transport in some legumes. Here, we investigated the role of root basipetal auxin transport during nodulation. Rhizobia inoculation significantly increased basipetal auxin transport in both Medicago truncatula and Lotus japonicus. In M. truncatula, this increase was dependent on functional Nod factor signalling through NFP, NIN, and NSP2, as well as ethylene signalling through SKL. To test whether increased basipetal auxin transport is required for nodulation, we examined a loss-of-function mutant of the M. truncatula PIN2 gene. The Mtpin2 mutant exhibited a reduction in basipetal auxin transport and an agravitropic phenotype. Inoculation of Mtpin2 roots with rhizobia still led to a moderate increase in basipetal auxin transport, but the mutant nodulated normally. No clear differences in auxin response were observed during nodule development. Interestingly, inoculation of wild-type roots increased lateral root numbers, whereas inoculation of Mtpin2 mutants resulted in reduced lateral root numbers compared with uninoculated roots. We conclude that the MtPIN2 auxin transporter is involved in basipetal auxin transport, that its function is not essential for nodulation, but that it plays an important role in the control of lateral root development.


2021 ◽  
Author(s):  
Pierre-Mathieu Pélissier ◽  
Hans Motte ◽  
Tom Beeckman

Abstract Lateral roots are important to forage for nutrients due to their ability to increase the uptake area of a root system. Hence, it comes as no surprise that lateral root formation is affected by nutrients or nutrient starvation, and as such contributes to the root system plasticity. Understanding the molecular mechanisms regulating root adaptation dynamics towards nutrient availability is useful to optimize plant nutrient use efficiency. There is at present a profound, though still evolving, knowledge on lateral root pathways. Here, we aimed to review the intersection with nutrient signaling pathways to give an update on the regulation of lateral root development by nutrients, with a particular focus on nitrogen. Remarkably, it is for most nutrients not clear how lateral root formation is controlled. Only for nitrogen, one of the most dominant nutrients in the control of lateral root formation, the crosstalk with multiple key signals determining lateral root development is clearly shown. In this update, we first present a general overview of the current knowledge of how nutrients affect lateral root formation, followed by a deeper discussion on how nitrogen signaling pathways act on different lateral root-mediating mechanisms for which multiple recent studies yield insights.


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