SCARECROW-LIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme

Gao, Ming‐Jun; Li, Xiang; Huang, Jun; Gropp, Gordon; Gjetvaj, Branimir; Lindsay, Donna L.; Shu, Wei; Coutu, Cathy; Chen, Zhixiang; Wan, Xiaochun; Hannoufa, Abdelali; Lydiate, Derek J.; Gruber, Margaret Y.; Chen, Z. Jeffrey; Hegedus, Dwayne D.

doi:10.1038/ncomms8243

Cited by 67 publications

(37 citation statements)

References 65 publications

(100 reference statements)

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“…2B). In contrast, crosses to drm2-2 or hda19-1t, a histone deacetylase that is functionally distinct from HDA6 (42,43), yielded no viable hisn6a-2 homozygous F2 progeny (Fig. 2B).…”

Section: Resultsmentioning

confidence: 99%

Hybrid incompatibility caused by an epiallele

Blevins

Wang

Pflieger

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Hybrid incompatibility resulting from deleterious gene combinations is thought to be an important step toward reproductive isolation and speciation. Here, we demonstrate involvement of a silent epiallele in hybrid incompatibility. In Arabidopsis thaliana accession Cvi-0, one of the two copies of a duplicated histidine biosynthesis gene, HISN6A, is mutated, making HISN6B essential. In contrast, in accession Col-0, HISN6A is essential because HISN6B is not expressed. Owing to these differences, Cvi-0 × Col-0 hybrid progeny that are homozygous for both Cvi-0 HISN6A and Col-0 HISN6B do not survive. We show that HISN6B of Col-0 is not a defective pseudogene, but a stably silenced epiallele. Mutating HISTONE DEACETYLASE 6 (HDA6), or the cytosine methyltransferase genes MET1 or CMT3, erases HISN6B's silent locus identity, reanimating the gene to circumvent hisn6a lethality and hybrid incompatibility. These results show that HISN6-dependent hybrid lethality is a revertible epigenetic phenomenon and provide additional evidence that epigenetic variation has the potential to limit gene flow between diverging populations of a species.gene silencing | epigenetic inheritance | DNA methylation | histone deacetylation | hybrid incompatibility M utations that accumulate in separate subpopulations of a species can facilitate reproductive isolation by engendering hybrid incompatibility, a reduction in fitness observed among hybrid progeny at the F1 or F2 generation (1-3). Bateson (4), Dobzhansky (5), and Muller (6) independently proposed that gene mutations made benign by compensatory mutations in interacting genes within isolated subpopulations prove deleterious when subpopulations or ecotypes interbreed, thereby contributing to speciation by reducing gene flow. Examples of this include the lethal consequences of a Saccharomyces cerevisiae protein directing improper splicing of essential Saccharomyces bayanus mRNAs in S. cerevisiae × S. bayanus hybrids (3) or the hybrid necrosis that results from expression of incompatible innate immune receptors in Arabidopsis thaliana (1).Lynch and Force (7) envisioned an alternative scenario by which hybrid incompatibilities might arise, as a result of gene duplication. Gene duplication initially results in gene redundancy, thereby relaxing constraints on sequence and functional divergence, but mutations most often transform one paralog into a nonfunctional pseudogene (8-10). Lynch and Force recognized that asymmetric resolution of gene duplicates in this manner could result in either paralog becoming the sole operational copy in different subpopulations of a species, such that hybrid progeny inheriting nonfunctional alleles of both subpopulations would suffer reduced fitness (7).Nonmutational (epigenetic) gene silencing could potentially contribute to hybrid incompatibility via the scenario envisioned by Lynch and Force. In plants, silent epialleles segregating in Mendelian fashion can be stably inherited over many generations, and are known to affect a number of well-studied traits, includin...

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“…2B). In contrast, crosses to drm2-2 or hda19-1t, a histone deacetylase that is functionally distinct from HDA6 (42,43), yielded no viable hisn6a-2 homozygous F2 progeny (Fig. 2B).…”

Section: Resultsmentioning

confidence: 99%

Hybrid incompatibility caused by an epiallele

Blevins

Wang

Pflieger

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The relationship between GA and GRAS proteins has been extensively studied (Sun et al ., ), but some GRAS proteins have also been found to be involved in auxin signalling. For instance, an auxin‐induced GRAS protein AtSCL15 plays crucial role during seed maturation programme (Gao et al ., ). The SCR/SHR complex comprised of two GRAS members has been proved to take part in root development by modulating both GA and auxin signalling (Heo et al ., ; Rovere et al ., ; Zhang et al ., ).…”

Section: Discussionmentioning

confidence: 97%

Overexpression of a tomato miR171 target gene SlGRAS24 impacts multiple agronomical traits via regulating gibberellin and auxin homeostasis

Huang

Peng

Xian

et al. 2016

Plant Biotechnology Journal

142

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SummaryIn Arabidopsis, the miR171‐GRAS module has been clarified as key player in meristem maintenance. However, the knowledge about its role in fruit crops like tomato (Solanum lycopersicum) remains scarce. We previously identified tomato SlGRAS24 as a target gene of Sly‐miR171. To study the role of this probable transcription factor, we generated transgenic tomato plants underexpressing SlGRAS24, overexpressing SlGRAS24, overexpressing Sly‐miR171 and expressing β‐glucuronidase (GUS) under the SlGRAS24 promoter (proSlGRAS24‐GUS). Plants overexpressing SlGRAS24 (SlGRAS24‐OE) had pleiotropic phenotypes associated with multiple agronomical traits including plant height, flowering time, leaf architecture, lateral branch number, root length, fruit set and development. Many GA/auxin‐related genes were down‐regulated and altered responsiveness to exogenous IAA/NAA or GA 3 application was observed in SlGRAS24‐OE seedlings. Moreover, compromised fruit set and development in SlGRAS24‐OE was also observed. These newly identified phenotypes for SlGRAS24 homologs in tomato were later proved to be caused by impaired pollen sacs and fewer viable pollen grains. At anthesis, the comparative transcriptome results showed altered expression of genes involved in pollen development and hormone signalling. Taken together, our data demonstrate that SlGRAS24 participates in a series of developmental processes through modulating gibberellin and auxin signalling, which sheds new light on the involvement of hormone crosstalk in tomato development.

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“…Viable hisn6a-2 homozygotes represented 20% of the F2 plants from the cmt3-11t cross and 11% of the F2 plants resulting from the met1-7 cross ( Figure 2B). By contrast, crosses to drm2-2 or hda19-t1, a histone deacetylase that is functionally distinct from HDA6 (41,42), yielded no viable hisn6a-2 homozygous F2 progeny ( Figure 2B). We conclude that HISN6B can be converted from a silent epiallele to an active allele in hda6, cmt3 or met1 mutants, allowing the re-animated gene to rescue plants lacking the normally essential HISN6A gene.…”

Section: Resultsmentioning

confidence: 99%