MicroRNA167-Directed Regulation of the Auxin Response Factors <i>GmARF8a</i> and <i>GmARF8b</i> Is Required for Soybean Nodulation and Lateral Root Development

Wang, Youning; Li, Kexue; Chen, Liang; Zou, Yanmin; Liu, Haipei; Tian, Yinping; Li, Dongxiao; Wang, Rui; Zhao, Fang; Ferguson, Brett J.; Gresshoff, Peter M.; Li, Xia

doi:10.1104/pp.15.00265

Cited by 169 publications

(132 citation statements)

References 88 publications

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“…In order to validate the role of miR393‐ GmTIR1/AFB3 ‐mediated auxin signaling and auxin response in soybean nodulation, we analyzed the effects of GmTIR1/AFB3 on transcription levels of GmIAAs ( GmIAA8 , GmIAA9 and GmIAA14 ) and GmARF8 ( GmARF8a and GmARF8b ) genes, which have been shown to mediate soybean nodulation (Turner et al ., ; Wang et al ., ). As shown in Fig.…”

Section: Resultsmentioning

confidence: 97%

“…It has been shown that increased auxin response is associated with de novo organogenesis of nodules in legumes as indicated by the expression of the auxin‐responsive marker genes, such as DR5pro:GUS and GH3pro:GUS in both indeterminate nodules (Mathesius et al ., ; Huo et al ., ; van Noorden et al ., ; Breakspear et al ., ) and determinate nodules (Pacios‐Bras et al ., ; Takanashi et al ., ; Turner et al ., ). Later functional studies showed that manipulation of miR160 and miR167, which target the genes encoding auxin response factors (ARF), altered nodulation in soybean (Turner et al ., ; Wang et al ., ). Here, we provided direct evidence for the involvement of auxin signaling and responses in soybean nodulation.…”

Section: Discussionmentioning

confidence: 97%

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GmTIR1/GmAFB3‐based auxin perception regulated by miR393 modulates soybean nodulation

et al. 2017

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Auxins play important roles in the nodulation of legumes. However, the mechanism by which auxin signaling regulates root nodulation is largely unknown. In particular, the role of auxin receptors and their regulation in determinate nodule development remains elusive. We checked the expression pattern of the auxin receptor GmTIR1/GmAFB3 genes in soybean. We analyzed the functions of GmTIR1/AFB3 in the regulation of rhizobial infection and nodule number, and also tested the functions of miR393 during nodulation and its relationship with GmTIR1/AFB3. The results showed that GmTIR1 and GmAFB3 genes exhibit diverse expression patterns during nodulation and overexpression of GmTIR1 genes significantly increased inflection foci and eventual nodule number. GmTIR1/AFB3 genes were post-transcriptionally cleaved by miR393 family and knock-down of the miR393 family members significantly increased rhizobial infection and the nodule number. Overexpression of the mutated form of GmTIR1C at the miR393 cleavage site that is resistant to miR393 cleavage led to a further increase in the number of infection foci and nodules, suggesting that miR393s modulate nodulation by directly targeting GmTIR1C. This study demonstrated that GmTIR1- and GmAFB3-mediated auxin signaling, that is spatio-temporally regulated by miR393, plays a crucial role in determinate nodule development in soybean.

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Section: Resultsmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

GmTIR1/GmAFB3‐based auxin perception regulated by miR393 modulates soybean nodulation

et al. 2017

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“…) and Glycine max (Wang et al . ), and predicted conserved binding sites and the presence of the respective miRNA loci have been shown for Populus trichocarpa (Kalluri et al . ), Eucalyptus grandis (Yu et al .…”

Section: Auxin Response Factors Are Also Regulated By Auxin‐independementioning

confidence: 99%

Auxin response factors

Chandler

2016

Plant Cell & Environment

223

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Auxin signalling involves the activation or repression of gene expression by a class of auxin response factor (ARF) proteins that bind to auxin response elements in auxin-responsive gene promoters. The release of ARF repression in the presence of auxin by the degradation of their cognate auxin/indole-3-acetic acid repressors forms a paradigm of transcriptional response to auxin. However, this mechanism only applies to activating ARFs, and further layers of complexity of ARF function and regulation are being revealed, which partly reflect their highly modular domain structure. This review summarizes our knowledge concerning ARF binding site specificity, homodimer and heterodimer multimeric ARF association and cooperative function and how activator ARFs activate target genes via chromatin remodelling and evolutionary information derived from phylogenetic comparisons from ARFs from diverse species. ARFs are regulated in diverse ways, and their importance in non-auxin-regulated pathways is becoming evident. They are also embedded within higher-order transcription factor complexes that integrate signalling pathways from other hormones and in response to the environment. The ways in which new information concerning ARFs on many levels is causing a revision of existing paradigms of auxin response are discussed.

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“…For example, exogenous auxin or enhanced sensitivity to auxin inhibited nodule formation in Medicago truncatula (Breakspear et al, ; Hobecker et al, ; van Noorden, Ross, Reid, Barry, & Ulrike, ) and conversely resistance to auxin resulted in enhanced nodule development in this species (Kuppusamy et al, ). In soybean, enhanced sensitivity to auxin resulted in reduced nodule formation (Wang et al, ) and was associated with reduced sensitivity to CK (Turner et al, ). Exogenous CK restored nodule numbers in these roots, suggesting that the underlying reason for reduced nodulation in auxin hypersensitive roots is reduced CK activity (Nizampatnam, Schreier, Damodaran, Adhikari, & Subramanian, ).…”

Section: Introductionmentioning

confidence: 99%

Quantitative 3D imaging of cell level auxin and cytokinin response ratios in soybean roots and nodules

et al. 2018

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Legume-Rhizobium symbiosis results in root nodules where rhizobia fix atmospheric nitrogen into plant usable forms in exchange for plant-derived carbohydrates. The development of these specialized root organs involves a set of carefully orchestrated plant hormone signalling. In particular, a spatio-temporal balance between auxin and cytokinin appears to be crucial for proper nodule development. We put together a construct that carried nuclear localized fluorescence sensors for auxin and cytokinin and used two photon induced fluorescence microscopy for concurrent quantitative 3-dimensional imaging to determine cellular level auxin and cytokinin outputs and ratios in root and nodule tissues of soybean. The use of nuclear localization signals on the markers and nuclei segmentation during image processing enabled accurate monitoring of outputs in 3D image volumes. The ratiometric method used here largely compensates for variations in individual outputs due to sample turbidity and scattering, an inherent issue when imaging thick root and nodule samples typical of many legumes. Overlays of determined auxin/cytokinin ratios on specific root zones and cell types accurately reflected those predicted based on previously reported outputs for each hormone individually. Importantly, distinct auxin/cytokinin ratios corresponded to distinct nodule cell types indicating a key role for these hormones in nodule cell type identity.

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MicroRNA167-Directed Regulation of the Auxin Response Factors GmARF8a and GmARF8b Is Required for Soybean Nodulation and Lateral Root Development

Cited by 169 publications

References 88 publications

GmTIR1/GmAFB3‐based auxin perception regulated by miR393 modulates soybean nodulation

GmTIR1/GmAFB3‐based auxin perception regulated by miR393 modulates soybean nodulation

Auxin response factors

Quantitative 3D imaging of cell level auxin and cytokinin response ratios in soybean roots and nodules

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