Interactions between ethylene, gibberellins, and brassinosteroids in the development of rhizobial and mycorrhizal symbioses of pea

Foo, Eloise; McAdam, Erin L.; Weller, James L.; Reid, James B.

doi:10.1093/jxb/erw047

Cited by 62 publications

(63 citation statements)

References 67 publications

(125 reference statements)

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“…ABA-related gene expression patterns indicated that the positive influence exerted by the mycorrhizal colonization on ABA biosynthesis and signaling (Herrera-Medina et al, 2007;Martín-Rodríguez et al, 2016), was not affected in the spr2 mutant. On the other hand, ET gene expression patterns concurred with ample evidence proposing that ET generally has an inhibitory effect on the AMF colonization (Foo et al, 2013(Foo et al, , 2016Pozo et al, 2015;Gomez Monteiro Fracetto, Pereira Peres & Rodriguez Lambais, 2017). Thus, the majority of the ET biosynthetic and signaling genes analyzed were induced in mycorrhizal spr2 roots, predominantly at 32 dpi.…”

Section: Ion Identitysupporting

confidence: 61%

“…BR-related genes were strongly repressed in mycorrhizal WT roots, while they were generally up-regulated in mycorrhizal spr2 roots. This was also in contradiction with the overall positive influence that BRs had in various plant models, including tomato (Bitterlich et al, 2014a(Bitterlich et al, , 2014bFoo et al, 2016;Tofighi et al, 2017). However, most of this information was obtained using BR-deficient mutants under experimental conditions that may have influenced other plant hormones (e.g., ethylene; Jiroutova, Oklestkova & Strnad, 2018), known to affect mycorrhizal colonization.…”

Section: Ion Identitymentioning

confidence: 89%

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Distinct gene expression and secondary metabolite profiles insuppressor of prosystemin-mediated responses2 (spr2)tomato mutants having impaired mycorrhizal colonization

Casarrubias-Castillo

Montero-Vargas

Dabdoub-González

et al. 2020

PeerJ

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Arbuscular mycorrhizal fungi (AMF) colonization, sampled at 32-50 days post-inoculation (dpi), was significantly reduced in suppressor of prosysteminmediated responses2 (spr2) mutant tomato plants impaired in the ω−3 FATTY ACID DESATURASE7 (FAD7) gene that limits the generation of linolenic acid and, consequently, the wound-responsive jasmonic acid (JA) burst. Contrary to wild-type (WT) plants, JA levels in root and leaves of spr2 mutants remained unchanged in response to AMF colonization, further supporting its regulatory role in the AM symbiosis. Decreased AMF colonization in spr2 plants was also linked to alterations associated with a disrupted FAD7 function, such as enhanced salicylic acid (SA) levels and SA-related defense gene expression and a reduction in fatty acid content in both mycorrhizal spr2 roots and leaves. Transcriptomic data revealed that lower mycorrhizal colonization efficiency in spr2 mutants coincided with the modified expression of key genes controlling gibberellin and ethylene signaling, brassinosteroid, ethylene, apocarotenoid and phenylpropanoid synthesis, and the wound response. Targeted metabolomic analysis, performed at 45 dpi, revealed augmented contents of L-threonic acid and DL-malic acid in colonized spr2 roots which suggested unfavorable conditions for AMF colonization. Additionally, timeand genotype-dependent changes in root steroid glycoalkaloid levels, including tomatine, suggested that these metabolites might positively regulate the AM symbiosis in tomato. Untargeted metabolomic analysis demonstrated that the tomato root metabolomes were distinctly affected by genotype, mycorrhizal colonization and colonization time. In conclusion, reduced AMF colonization efficiency in spr2 mutants is probably caused by multiple and interconnected JA-dependent and independent gene expression and metabolomic alterations.How to cite this article Casarrubias-Castillo K, Montero-Vargas JM, Dabdoub-González N, Winkler R, Martinez-Gallardo NA, Zañudo-Hernández J, Avilés-Arnaut H, Délano-Frier JP. 2020. Distinct gene expression and secondary metabolite profiles in suppressor of prosystemin-mediated responses2 (spr2) tomato mutants having impaired mycorrhizal colonization. PeerJ 8:e8888 . 2012. Loss of function of fatty acid desaturase 7 in tomato enhances basal aphid resistance in a salicylate-dependent manner.

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Section: Ion Identitysupporting

confidence: 61%

Section: Ion Identitymentioning

confidence: 89%

Distinct gene expression and secondary metabolite profiles insuppressor of prosystemin-mediated responses2 (spr2)tomato mutants having impaired mycorrhizal colonization

Casarrubias-Castillo

Montero-Vargas

Dabdoub-González

et al. 2020

PeerJ

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“…Ethylene signaling is a key regulator of rhizobia infection and nodule organogenesis, as mutants in Ein2 are hypernodulating and hyperinfected (Penmetsa and Cook, 1997;Penmetsa et al, 2008;Foo et al, 2016).…”

mentioning

confidence: 99%

Dynamics of Ethylene Production in Response to Compatible Nod Factor

et al. 2017

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Establishment of symbiotic nitrogen-fixation in legumes is regulated by the plant hormone ethylene, but it has remained unclear whether and how its biosynthesis is regulated by the symbiotic pathway. We established a sensitive ethylene detection system for Lotus japonicus and found that ethylene production increased as early as 6 hours after inoculation with Mesorhizobium loti. This ethylene response was dependent on Nod factor production by compatible rhizobia. Analyses of nodulation mutants showed that perception of Nod factor was required for ethylene emission, while downstream transcription factors including CYCLOPS, NIN, and ERN1 were not required for this response. Activation of the nodulation signaling pathway in spontaneously nodulating mutants was also sufficient to elevate ethylene production. Ethylene signaling is controlled by EIN2, which is duplicated in L. japonicus. We obtained a L. japonicus Ljein2a Ljein2b double mutant that exhibits complete ethylene insensitivity and confirms that these two genes act redundantly in ethylene signaling. Consistent with this redundancy, both LjEin2a and LjEin2b are required for negative regulation of nodulation and Ljein2a Ljein2b double mutants are hypernodulating and hyperinfected. We also identified an unexpected role for ethylene in the onset of nitrogen fixation, with the Ljein2a Ljein2b double mutant showing severely reduced nitrogen fixation. These results demonstrate that ethylene production is an early and sustained nodulation response that acts at multiple stages to regulate infection, nodule organogenesis, and nitrogen fixation in L. japonicus.

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“…Previously, more nodules of smaller size were observed in the Mm SWRI9‐inoculated association than in Mc CP‐31‐inoculated association during low‐Pi supply, which coincided with lower SNF capacity of Mm SWRI9‐inoculated plants than that of the Mc CP‐31‐inoculated plants under Pi‐deficient conditions (Nasr Esfahani et al ., ). It has recently been reported that the pea ( Pisum sativum ) ethylene (ET)‐insensitive and gibberellin (GA)‐deficient double mutant ein2 na and ET‐insensitive and brassinosteroid (BR)‐deficient double mutant ein2 lk produced more nodules of smaller size compared with wild‐type plants (Foo et al ., ). Our RNA‐seq data analysis revealed differential expression patterns of hormone‐related genes obtained from Mm SWRI9‐Pd/ Mm SWRI9‐Ps and Mc CP‐31‐Pd/ Mc CP‐31‐Ps comparisons (Figure S1).…”

Section: Resultsmentioning

confidence: 97%

Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency

et al. 2017

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Phosphate (Pi) deficiency is known to be a major limitation for symbiotic nitrogen fixation (SNF), and hence legume crop productivity globally. However, very little information is available on the adaptive mechanisms, particularly in the important legume crop chickpea (Cicer arietinum L.), which enable nodules to respond to low-Pi availability. Thus, to elucidate these mechanisms in chickpea nodules at molecular level, we used an RNA sequencing approach to investigate transcriptomes of the nodules in Mesorhizobium mediterraneum SWRI9-(MmSWRI9)-chickpea and M. ciceri CP-31-(McCP-31)-chickpea associations under Pi-sufficient and Pi-deficient conditions, of which the McCP-31-chickpea association has a better SNF capacity than the MmSWRI9-chickpea association during Pi starvation. Our investigation revealed that more genes showed altered expression patterns in MmSWRI9-induced nodules than in McCP-31-induced nodules (540 vs. 225) under Pi deficiency, suggesting that the Pi-starvation-more-sensitive MmSWRI9-induced nodules required expression change in a larger number of genes to cope with low-Pi stress than the Pi-starvation-less-sensitive McCP-31-induced nodules. The functional classification of differentially expressed genes (DEGs) was examined to gain an understanding of how chickpea nodules respond to Pi starvation, caused by soil Pi deficiency. As a result, more DEGs involved in nodulation, detoxification, nutrient/ion transport, transcriptional factors, key metabolic pathways, Pi remobilization and signalling were found in Pi-starved MmSWRI9-induced nodules than in Pi-starved McCP-31-induced nodules. Our findings have enabled the identification of molecular processes that play important roles in the acclimation of nodules to Pi deficiency, ultimately leading to the development of Pi-efficient chickpea symbiotic associations suitable for Pi-deficient soils.

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Interactions between ethylene, gibberellins, and brassinosteroids in the development of rhizobial and mycorrhizal symbioses of pea

Abstract: HighlightAn ethylene-insensitive mutant of pea with enhanced nodulation and arbuscular mycorrhizal development showed that gibberellin and brassinosteroid deficiency affect nodule number via ethylene levels.

Cited by 62 publications

References 67 publications

Distinct gene expression and secondary metabolite profiles insuppressor of prosystemin-mediated responses2 (spr2)tomato mutants having impaired mycorrhizal colonization

Distinct gene expression and secondary metabolite profiles insuppressor of prosystemin-mediated responses2 (spr2)tomato mutants having impaired mycorrhizal colonization

Dynamics of Ethylene Production in Response to Compatible Nod Factor

Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency

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