<i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both

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....

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Main Authors: Jack Colicchio, John Kelly, Lena Hileman
Format: Article
Language:English
Published: MDPI AG 2020-10-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/20/7552
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author Jack Colicchio
John Kelly
Lena Hileman
author_facet Jack Colicchio
John Kelly
Lena Hileman
author_sort Jack Colicchio
collection DOAJ
description 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 <i>Mimulus guttatus</i>. Here, we sequenced <i>M. guttatus</i> 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 <i>a priori</i> 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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spelling doaj.art-d56008501ea9493a930b7ec0d2423b062023-11-20T16:53:30ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-10-012120755210.3390/ijms21207552<i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely BothJack Colicchio0John Kelly1Lena Hileman2Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USAEcology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USAEcology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USAOrganisms 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 <i>Mimulus guttatus</i>. Here, we sequenced <i>M. guttatus</i> 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 <i>a priori</i> 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.https://www.mdpi.com/1422-0067/21/20/7552small RNAsepigeneticstransgenerational plasticitywound-responsetRFs<i>Mimulus guttatus</i>
spellingShingle Jack Colicchio
John Kelly
Lena Hileman
<i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both
International Journal of Molecular Sciences
small RNAs
epigenetics
transgenerational plasticity
wound-response
tRFs
<i>Mimulus guttatus</i>
title <i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both
title_full <i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both
title_fullStr <i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both
title_full_unstemmed <i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both
title_short <i>Mimulus</i> sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both
title_sort i mimulus i srnas are wound responsive and associated with transgenerationally plastic genes but rarely both
topic small RNAs
epigenetics
transgenerational plasticity
wound-response
tRFs
<i>Mimulus guttatus</i>
url https://www.mdpi.com/1422-0067/21/20/7552
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AT johnkelly imimulusisrnasarewoundresponsiveandassociatedwithtransgenerationallyplasticgenesbutrarelyboth
AT lenahileman imimulusisrnasarewoundresponsiveandassociatedwithtransgenerationallyplasticgenesbutrarelyboth