The evolution of determinate and indeterminate nodules within the Papilionoideae subfamily

Ren, Gui-Ling

doi:10.18174/429101

Cited by 8 publications

(16 citation statements)

References 71 publications

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“…(2) The root nodule primordium is formed by restoring the meristematic capacity of the endothelial parenchyma cells immediately outside the pericycle, and the lateral roots still originate from the pericycle cells. Ren et al . (2018) advised that nodules originate from the cortical cells of roots.…”

Section: Discussionmentioning

confidence: 99%

“…Root nodules can be divided into two types, i.e., determinate nodules and indeterminate nodules (Kazuhiko, 2011), the former of which have no meristem or secondary growth and are often nearly spherical in shape, and fast-growing root nodules of legumes mostly belong to this type. The latter type has internal meristems and can undergo secondary growth, the nodules often have branching phenomena, and the nodules of alfalfa, pea, clover, bayberry, alder, and other plants belong to this type (Kazuhiko, 2011; Ren, 2018). According to the above classification, the P. macrophyllus root nodules formed on young and old roots are finite nodules, while the nodules formed on senescent nodules are infinite nodules.…”

Section: Discussionmentioning

confidence: 99%

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Microscopic and ultramicroscopic anatomical characteristics of root nodules in Podocarpus macrophyllus during development

Li-qiong

Chen

Zhao

et al. 2022

Preprint

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To understand the morphological and structural characteristics of root nodules in Podocarpus macrophyllus and their development, this study prepared P. macrophyllus root nodule samples at the young, mature, and senescent stages. Optical microscopy and transmission electron microscopy (SEM) revealed that new nodules can be formed on roots and senescent nodules; new nodules formed on the roots are nearly spherical and have an internal structure similar to finite nodules; new nodules on senescent nodules are formed by extension and differentiation of the vascular cylinder of the original nodules; and these new nodules are nested at the base of the original nodules, which create growth space for new nodules by dissociating the cortical tissue; clusters of nodules are formed after extensive accumulation, and the growth pattern is similar to that of infinite nodules; the symbiotic bacteria of P. macrophyllus root nodules mainly invade from the epidermal intercellular space of the roots and migrate along the intercellular space of the nodule cortex; infected nodule cortex cells have a well-developed inner membrane system and enlarged and loose nuclei; and unique Frankia vesicles, and rhizobia cysts, and bacteriophages can all develop. Compared with common leguminous and nonleguminous plant nodules, P. macrophyllus root nodules are more complex in morphology, structure and composition. From the perspective of plant system evolution, the rhizobium nodules in leguminous angiosperms and Frankia nodules in nonleguminous angiosperms are most likely two branches derived from the nodules in gymnosperms, such as P. macrophyllus. The conclusions of this study can provide a theoretical basis for the developmental biology of P. macrophyllus root nodules and the evolutionary pattern of plant symbionts.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Microscopic and ultramicroscopic anatomical characteristics of root nodules in Podocarpus macrophyllus during development

Li-qiong

Chen

Zhao

et al. 2022

Preprint

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“…By contrast, IDN of L. leucocephala possess a persistent apical meristem and bacteria that are released from infection threads into plant cells that have stopped dividing will only divide a few times before differentiating into nitrogen-fixing bacteroids (Oke and Long, 1999). Recently, IDN of Indigofera and Tephrosia species were reclassified as DN that develop from the outermost root cortical cells and have, instead of persistent meristems, secondary clusters of dividing nodule cells some of which contain infection threads (Ren, 2018). Whether the differences in the infection process and ontogeny of determinate versus indeterminate nodules may explain the distinct symbiotic phenotypes of NGRΔrRNA1,3 on V. unguiculata and L. leucocephala remains to be explored.…”

Section: Discussionmentioning

confidence: 99%

“…As bacteroids of DN are not terminally differentiated, most rhizobia can resume a free-living growth in soils once nodules senesce and disaggregate. Recently, plants of the Indigofera and Tephrosia genera that were initially thought to form IDN, were reported to make nodules that carry secondary clusters of dividing cells instead of a persistent meristem (Ren, 2018). Yet, regardless of the strain or type of nodule considered, rhizobia must first efficiently colonize the plant rhizosphere, multiply within growing ITs, circumvent or withstand plant defenses, colonize and establish persistent colonies inside nodules cells, before becoming proficient symbionts.…”

Section: Introductionmentioning

confidence: 99%

Deletion of rRNA Operons of Sinorhizobium fredii Strain NGR234 and Impact on Symbiosis With Legumes

Cherni

Perret

2019

Front. Microbiol.

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During their lifecycle, from free-living soil bacteria to endosymbiotic nitrogen-fixing bacteroids of legumes, rhizobia must colonize, and cope with environments where nutrient concentrations and compositions vary greatly. Bacterial colonization of legume rhizospheres and of root surfaces is subject to a fierce competition for plant exudates. By contrast root nodules offer to rhizobia sheltered nutrient-rich environments within which the cells that successfully propagated via infection threads can rapidly multiply. To explore the effects on symbiosis of a slower rhizobia growth and metabolism, we deleted one or two copies of the three functional rRNA operons of the promiscuous Sinorhizobium fredii strain NGR234 and examined the impact of these mutations on free-living and symbiotic lifestyles. Strains with two functional rRNA operons (NGRΔrRNA1 and NGRΔrRNA3) grew almost as rapidly as NGR234, and NGRΔrRNA1 was as proficient as the parent strain on all of the five legume species tested. By contrast, the NGRΔrRNA1,3 double mutant, which carried a single rRNA operon and grew significantly slower than NGR234, had a reduced symbiotic proficiency on Cajanus cajan, Macroptilium atropurpureum, Tephrosia vogelii , and Vigna unguiculata . In addition, while NGRΔrRNA1 and NGR234 equally competed for nodulation of V. unguiculata , strain NGRΔrRNA1,3 was clearly outcompeted by wild-type. Surprisingly, on Leucaena leucocephala , NGRΔrRNA1,3 was the most proficient strain and competed equally NGR234 for nodule occupation. Together, these results indicate that for strains with otherwise identical repertoires of symbiotic genes, a faster growth on roots and/or inside plant tissues may contribute to secure access to nodules of some hosts. By contrast, other legumes such as L. leucocephala appear as less selective and capable of providing symbiotic environments susceptible to accommodate strains with a broader spectrum of competences.

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“…Cowpea (Vigna unguiculata), siratro (Macroptilium atropurpureum) and soybean (Glycine max) are examples of legumes crops with DN. With time, some DN may also develop secondary clusters of dividing cells that form new nodule meristems, as was shown for Tephrosia vogelii (and by analogy Cajanus cajan) [10]. The developmental and infection processes leading to the formation of proficient nodules where bacteroids can fix nitrogen are complex, and sets of molecular cues exchanged by plants and rhizobia coordinate both of these processes [11,12].…”

Section: Introductionmentioning

confidence: 87%

A Minimal Genetic Passkey to Unlock Many Legume Doors to Root Nodulation by Rhizobia

Unay

Perret

2020

Genes

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In legume crops, formation of developmentally mature nodules is a prerequisite for efficient nitrogen fixation by populations of rhizobial bacteroids established inside nodule cells. Development of root nodules, and concomitant microbial colonization of plant cells, are constrained by sets of recognition signals exchanged by infecting rhizobia and their legume hosts, with much of the specificity of symbiotic interactions being determined by the flavonoid cocktails released by legume roots and the strain-specific nodulation factors (NFs) secreted by rhizobia. Hence, much of Sinorhizobium fredii strain NGR234 symbiotic promiscuity was thought to stem from a family of >80 structurally diverse NFs and associated nodulation keys in the form of secreted effector proteins and rhamnose-rich surface polysaccharides. Here, we show instead that a mini-symbiotic plasmid (pMiniSym2) carrying only the nodABCIJ, nodS and nodD1 genes of NGR234 conferred promiscuous nodulation to ANU265, a derivative strain cured of the large symbiotic plasmid pNGR234a. The ANU265::pMiniSym2 transconjugant triggered nodulation responses on 12 of the 22 legumes we tested. On roots of Macroptilium atropurpureum, Leucaena leucocephala and Vigna unguiculata, ANU265::pMiniSym2 formed mature-like nodule and successfully infected nodule cells. While cowpea and siratro responded to nodule colonization with defense responses that eventually eliminated bacteria, L. leucocephala formed leghemoglobin-containing mature-like nodules inside which the pMiniSym2 transconjugant established persistent intracellular colonies. These data show seven nodulation genes of NGR234 suffice to trigger nodule formation on roots of many hosts and to establish chronic infections in Leucaena cells.

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The evolution of determinate and indeterminate nodules within the Papilionoideae subfamily

Cited by 8 publications

References 71 publications

Microscopic and ultramicroscopic anatomical characteristics of root nodules in Podocarpus macrophyllus during development

Microscopic and ultramicroscopic anatomical characteristics of root nodules in Podocarpus macrophyllus during development

Deletion of rRNA Operons of Sinorhizobium fredii Strain NGR234 and Impact on Symbiosis With Legumes

A Minimal Genetic Passkey to Unlock Many Legume Doors to Root Nodulation by Rhizobia

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