Plant RNases T2, but not Dicer-like proteins, are major players of tRNA-derived fragments biogenesis

Megel, Cyrille; Hummel, Guillaume; Lalande, Stéphanie; Ubrig, Élodie; Cognat, Valérie; Morelle, Geoffrey; Salinas‐Giegé, Thalia; Duchêne, Anne‐Marie; Maréchal-Drouard, Laurence

doi:10.1093/nar/gky1156

Cited by 104 publications

(127 citation statements)

References 48 publications

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“…RNS1 is markedly promoted by Pi deficit and RNS1 protein accumulates in the secretome of Pi starved cells (Tran and Plaxton, 2008). RNS1 expression is also associated to wounding induced local and systemic signaling (Lebrasseur et al, 2002), and correlates with the accumulation of specific tRNA fragments (Megel et al, 2019). The role of the other identified ribonuclease, PR4, is less known, its expression is associated with SAR (Mishina and Zeier, 2007), and its induced by ethylene and SA (Potter et al, 1993;Camargo-Ramírez et al, 2018).…”

Section: Proteins That Accumulate In the Apoplast Of Senescent Leavesmentioning

confidence: 99%

Physiological and Proteomic Changes in the Apoplast Accompany Leaf Senescence in Arabidopsis

et al. 2020

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The apoplast, i.e. the cellular compartment external to the plasma membrane, undergoes important changes during senescence. Apoplastic fluid volume increases quite significantly in senescing leaves, thereby diluting its contents. Its pH elevates by about 0.8 units, similar to the apoplast alkalization in response to abiotic stresses. The levels of 159 proteins decrease, whereas 24 proteins increase in relative abundance in the apoplast of senescing leaves. Around half of the apoplastic proteins of non-senescent leaves contain a N-terminal signal peptide for secretion, while all the identified senescence-associated apoplastic proteins contain the signal peptide. Several of the apoplastic proteins that accumulate during senescence also accumulate in stress responses, suggesting that the apoplast may constitute a compartment where developmental and stress-related programs overlap. Other senescence-related apoplastic proteins are involved in cell wall modifications, proteolysis, carbohydrate, ROS and amino acid metabolism, signaling, lipid transport, etc. The most abundant senescence-associated apoplastic proteins, PR2 and PR5 (e.g. pathogenesis related proteins PR2 and PR5) are related to leaf aging rather than to the chloroplast degradation program, as their levels increase only in leaves undergoing developmental senescence, but not in dark-induced senescent leaves. Changes in the apoplastic space may be relevant for signaling and molecular trafficking underlying senescence.

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Section: Proteins That Accumulate In the Apoplast Of Senescent Leavesmentioning

confidence: 99%

Physiological and Proteomic Changes in the Apoplast Accompany Leaf Senescence in Arabidopsis

et al. 2020

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“…This variation suggests that tRF-mediated responses are likely regulated by a number of down-stream processes. tRFs appear to be primarily produced by RNases involving both dicer dependent and dicer independent mechanisms [ 70 ] function through diverse mechanisms to mediate post-transcriptional and translational silencing [ 47 ] and are ubiquitous across all forms of life [ 71 ]. Once thought of as simply responsible for mediating translation, it is becoming clear that tRNAs associated pathways play important roles in modifying life history traits.…”

Section: Discussionmentioning

confidence: 99%

Mimulus sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both

Colicchio

Kelly

Hileman

2020

IJMS

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Organisms alter development in response to environmental cues. Recent studies demonstrate that they can transmit this plasticity to progeny. While the phenotypic and transcriptomic evidence for this “transgenerational plasticity” has accumulated, genetic and developmental mechanisms remain unclear. Plant defenses, gene expression and DNA methylation are modified as an outcome of parental wounding in Mimulus guttatus. Here, we sequenced M. guttatus small RNAs (sRNA) to test their possible role in mediating transgenerational plasticity. We sequenced sRNA populations of leaf-wounded and control plants at 1 h and 72 h after damage and from progeny of wounded and control parents. This allowed us to test three components of an a priori model of sRNA mediated transgenerational plasticity—(1) A subset of sRNAs will be differentially expressed in response to wounding, (2) these will be associated with previously identified differentially expressed genes and differentially methylated regions and (3) changes in sRNA abundance in wounded plants will be predictive of sRNA abundance, DNA methylation, and/or gene expression shifts in the following generation. Supporting (1) and (2), we found significantly different sRNA abundances in wounded leaves; the majority were associated with tRNA fragments (tRFs) rather than small-interfering RNAs (siRNA). However, siRNAs responding to leaf wounding point to Jasmonic Acid mediated responses in this system. We found that different sRNA classes were associated with regions of the genome previously found to be differentially expressed or methylated in progeny of wounded plants. Evidence for (3) was mixed. We found that non-dicer sRNAs with increased abundance in response to wounding tended to be nearby genes with decreased expression in the next generation. Counter to expectations, we did not find that siRNA responses to wounding were associated with gene expression or methylation changes in the next generation and within plant and transgenerational sRNA plasticity were negatively correlated.

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“…This is not surprising since RNase A family is vertebrate-specific, yet stress-induced tRNA cleavage is a well-conserved phenomenon in organisms that do not have RNase A. For example, In Tetrahymena, S. cerevisiae and Arabidopsis, stress-induced generation of tRNA halves has been attributed to the RNase T2 family (12,68,69). In mammalian cells, other RNases have also been described to cleave tRNAs, such as Dicer (70-72), RNase 1 (36), RNase L (73) and Schlafen13/SFLN13 (74).…”

Section: Discussionmentioning

confidence: 99%

The role of ANGIOGENIN, or lack thereof, in the generation of stress-induced tRNA halves and of smaller tRNA fragments that enter Argonaute complexes

Kuscu

Malik

et al. 2019

Preprint

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Overexpressed Angiogenin (ANG) cleaves tRNA anticodons to produce tRNA halves similar to those produced in response to stress, but it is not clear whether endogenous ANG is essential for producing the stress-induced tRNA halves. It is also not clear whether smaller tRNA fragments (tRFs) are generated from the tRNA halves. Global short RNAseq experiments reveal that ANG overexpression selectively cleaves a subset of tRNAs (tRNA Glu , tRNA Gly , tRNA Lys , tRNA Val , tRNA His , tRNA Asp and tRNA SeC ) to produce tRNA halves and 26-30 bases long tRF-5s. Surprisingly, knockout of ANG reveals that the majority of stress-induced tRNA halves except 5' half from tRNA HisGTG and 3' half from tRNA AspGTC are ANGindependent, suggesting there are other RNases that can produce tRNA halves. The 17-25 bases long tRF-3s and tRF-5s that could enter into Argonaute complexes are not induced by ANG overexpression, suggesting that they are generated independently from tRNA halves. Consistent with this, knockout of ANG did not decrease tRF-3 levels or gene-silencing activity. Therefore ANG cleaves specific tRNAs, is not the only RNAse that creates tRNA halves and the shorter tRFs are not generated from the tRNA halves or from independent tRNA cleavage by ANG.

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Plant RNases T2, but not Dicer-like proteins, are major players of tRNA-derived fragments biogenesis

Cited by 104 publications

References 48 publications

Physiological and Proteomic Changes in the Apoplast Accompany Leaf Senescence in Arabidopsis

Physiological and Proteomic Changes in the Apoplast Accompany Leaf Senescence in Arabidopsis

Mimulus sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both

The role of ANGIOGENIN, or lack thereof, in the generation of stress-induced tRNA halves and of smaller tRNA fragments that enter Argonaute complexes

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