Abstract
MicroRNA319 (miR319) and its targets TEOSINTE-BRANCHED1/CYCLOIDEA/PCF (TCP) transcription factors are well-characterized regulators of leaf and flower development, yet their role in root development remains elusive. Here, we demonstrated that overexpression of miR319a led to a decrease in the number and density of lateral roots in poplar, while repressing miR319a by short tandem target mimics (STTM) promoted lateral root (LR) development. The auxin signaling repressors IAA3.1 and IAA3.2 were upregulated in miR319a-OE plants but downregulated in miR319a-STTM plants. After exogenous applications of naphthaleneacetic acid (NAA), which exhibited the characteristics and physiological functions of the endogenous auxin indole-3-acetic acid, the number and density of LR in WT increased by 30% and 44%, respectively. In miR319a-OE plants, the LR number increased by 23% and 48%, and the LR density increased by 10% and 26%. NAA treatment can partially compensate for the phenotype of inhibited LR development caused by the overexpression of miR319a. After N-1-naphthylphthalamic acid (NPA) treatment, which is a key inhibitor of the directional (polar) transport of the auxin hormone in plants, the LR number in WT decreased by 70%. In the overexpression plants, the number of lateral roots decreased by 85–87%, and in the STTM plants, the number of lateral roots decreased by about 83%. It was proved that NPA treatment could reverse the phenotype of increased LR number in miR319a-STTM plants. Expression analysis revealed that miR319a significantly inhibited the expression of the key auxin-regulated genes IAA3.1 and IAA3.2, suggesting that auxin signaling might mediate its effects on lateral root formation. Additionally, we compared the fluorescence signal in the reporter line with GFP expression driven by the auxin-responsive DR5 promoter within the genetic backgrounds of WT, miR319a-OE, and miR319a-STTM plants, which revealed that auxin signaling was stronger in the epidermal cells and elongation zone cells in the LR of miR319a-OE plants, whereas in LR of WT and miR319a-STTM plants, auxin signaling was more pronounced in the root tip meristematic cells. Furthermore, transactivation assays and expression analysis indicated that IAA3.2 was a downstream target of TCP19. Chromatin immunoprecipitation coupled with quantitative PCR (ChIP-qPCR) confirmed that TCP19 directly bound to the promoter region of IAA3.2. These findings establish that miR319a targeted and cleaved TCP19, and TCP19 further directly and negatively regulates the expression of IAA3.2, thereby controlling LR development in Populus tomentosa (P. tomentosa). The formation of LR can expand the plant root system, which is of great significance for the vegetative propagation of plants and the in-vitro regeneration of explants. Moreover, the formation of LR is an important strategy for plants to cope with environmental stresses. This study provides a theoretical basis for breeding poplars more suitable for vegetative propagation.
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Claims 18
Claim · model-written summary
miR319a overexpression reduced poplar lateral root number and density.
- Treatment
- overexpression of miR319ae0
- Gene
- miR319ae0
- Outcome
- number and density of lateral rootse0
- Direction
- decreasee0
PopulusNot reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“overexpression of miR319a led to a decrease in the number and density of lateral roots in poplar”
Claim · model-written summary
miR319a repression promoted lateral root development.
- Taxon
- Populus tomentosa
Populus tomentosat0 - Treatment
- short tandem target mimics (STTM)e0
- Gene
- miR319ae0
- Outcome
- lateral root (LR) developmente0
- Direction
- promotede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“repressing miR319a by short tandem target mimics (STTM) promoted lateral root (LR) development”
t0“Populus tomentosa”
Claim · model-written summary
IAA3.1 and IAA3.2 were upregulated in miR319a-OE plants.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- miR319a-OEe0
- Gene
- IAA3.1 and IAA3.2e0
- Outcome
- IAA3.1 and IAA3.2e0
- Direction
- upregulatede0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“IAA3.1 and IAA3.2 were upregulated in miR319a-OE plants”
t0“Populus tomentosa”
Claim · model-written summary
IAA3.1 and IAA3.2 were downregulated in miR319a-STTM plants.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- miR319a-STTMe0
- Gene
- IAA3.1 and IAA3.2e0
- Outcome
- IAA3.1 and IAA3.2e0
- Direction
- downregulatede0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“IAA3.1 and IAA3.2 were upregulated in miR319a-OE plants but downregulated in miR319a-STTM plants”
t0“Populus tomentosa”
Claim · model-written summary
NAA increased wild-type lateral root number by 30%.
Not reportedTreatmentComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“number and density of LR in WT increased by 30% and 44%, respectively”
t0“Populus tomentosa”
Claim · model-written summary
NAA increased wild-type lateral root density by 44%.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- WTe0
- Outcome
- density of LRe0
- Direction
- increasede0
- Value
- 44%e0
Not reportedTreatmentComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“number and density of LR in WT increased by 30% and 44%, respectively”
t0“Populus tomentosa”
Claim · model-written summary
NAA increased lateral root number in miR319a-OE plants by 23% and 48%.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- miR319a-OEe0
- Outcome
- LR numbere0
- Direction
- increasede0
- Value
- 23% and 48%e0
Not reportedTreatmentComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In miR319a-OE plants, the LR number increased by 23% and 48%”
t0“Populus tomentosa”
Claim · model-written summary
NAA increased lateral root density in miR319a-OE plants by 10% and 26%.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- miR319a-OEe0
- Outcome
- LR densitye0
- Direction
- increasede0
- Value
- 10% and 26%e0
Not reportedTreatmentComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In miR319a-OE plants, the LR number increased by 23% and 48%, and the LR density increased by 10% and 26%”
t0“Populus tomentosa”
Claim · model-written summary
NPA decreased wild-type lateral root number by 70%.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- WTe0
- Outcome
- LR numbere0
- Direction
- decreasede0
- Value
- 70%e0
Not reportedTreatmentComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“LR number in WT decreased by 70%”
t0“Populus tomentosa”
Claim · model-written summary
NPA decreased lateral root number in overexpression plants by 85–87%.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- overexpression plantse0
- Outcome
- number of lateral rootse0
- Direction
- decreasede0
- Value
- 85–87%e0
Not reportedTreatmentComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In the overexpression plants, the number of lateral roots decreased by 85–87%”
t0“Populus tomentosa”
Claim · model-written summary
NPA decreased lateral root number in STTM plants by about 83%.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- STTM plantse0
- Outcome
- number of lateral rootse0
- Direction
- decreasede0
- Value
- about 83%e0
Not reportedTreatmentComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“in the STTM plants, the number of lateral roots decreased by about 83%”
t0“Populus tomentosa”
Claim · model-written summary
miR319a significantly inhibited IAA3.1 and IAA3.2 expression.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Gene
- IAA3.1 and IAA3.2e0
- Outcome
- expressione0
- Direction
- inhibitede0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“miR319a significantly inhibited the expression of the key auxin-regulated genes IAA3.1 and IAA3.2”
t0“Populus tomentosa”
Claim · model-written summary
Auxin signaling was stronger in epidermal and elongation-zone cells of miR319a-OE lateral roots.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- miR319a-OEe0
- Organ / stage
- epidermal cells and elongation zone cellse0
- Outcome
- auxin signalinge0
- Direction
- strongere0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“auxin signaling was stronger in the epidermal cells and elongation zone cells in the LR of miR319a-OE plants”
t0“Populus tomentosa”
Claim · model-written summary
Auxin signaling was more pronounced in root tip meristematic cells of WT and miR319a-STTM roots.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Material
- miR319a-STTMe0
- Organ / stage
- root tip meristematic cellse0
- Outcome
- auxin signalinge0
- Direction
- more pronouncede0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“in LR of WT and miR319a-STTM plants, auxin signaling was more pronounced in the root tip meristematic cells”
t0“Populus tomentosa”
Claim · model-written summary
IAA3.2 was identified as a downstream target of TCP19.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Gene
- IAA3.2e0
- Outcome
- downstream target of TCP19e0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“IAA3.2 was a downstream target of TCP19”
t0“Populus tomentosa”
Claim · model-written summary
TCP19 directly bound the IAA3.2 promoter.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Gene
- TCP19e0
- Outcome
- bound to the promoter region of IAA3.2e0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“TCP19 directly bound to the promoter region of IAA3.2”
t0“Populus tomentosa”
Claim · model-written summary
miR319a targeted and cleaved TCP19.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Gene
- miR319ae0
- Outcome
- targeted and cleaved TCP19e0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“miR319a targeted and cleaved TCP19”
t0“Populus tomentosa”
Claim · model-written summary
TCP19 directly and negatively regulated IAA3.2 expression and lateral root development.
- Taxon
- Populus tomentosaPopulus tomentosat0
- Gene
- TCP19e0
- Outcome
- expression of IAA3.2e0
- Direction
- negativelye0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“TCP19 further directly and negatively regulates the expression of IAA3.2, thereby controlling LR development”
t0“Populus tomentosa”