Transcriptional landscapes of floral meristems in barley

Thiel, Johannes; Koppolu, Ravi; Trautewig, Corinna; Hertig, Christian; Kale, Sandip M.; Erbe, S.; Mascher, Martin; Himmelbach, Axel; Rutten, Twan; Esteban, Eddi; Pasha, Asher; Kumlehn, Jochen; Provart, Nicholas J.; Vanderauwera, Sandy; Frohberg, Claus; Schnurbusch, Thorsten

doi:10.1126/sciadv.abf0832

Cited by 36 publications

(28 citation statements)

References 98 publications

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“…In contrast to this ancient role in vegetative branching, carpel suppression arose later and repeatedly in the grasses, for example, in the lineages leading to maize and barley ( Hordeum vulgare ) ( 3 , 53 , 54 ). Strikingly, floral organ suppression in barley is also mediated by a GT1 paralog, SIX-ROWED SPIKE1 ( VRS1 ), and an RA3 homolog is down-regulated in barley floral organ suppression mutants ( 54 – 59 ). Critically, while VRS1 does have a particular role in barley carpel suppression, it also acts to suppress the growth of other floral organs in lateral spikelets, and barley carpel suppression does not involve programmed cell death ( 58 , 59 ).…”

Section: Discussionmentioning

confidence: 99%

Recruitment of an ancient branching program to suppress carpel development in maize flowers

Klein

Gallagher

Demesa-Arévalo

et al. 2022

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

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Carpels in maize undergo programmed cell death in half of the flowers initiated in ears and in all flowers in tassels. The HD-ZIP I transcription factor gene GRASSY TILLERS1 (GT1) is one of only a few genes known to regulate this process. To identify additional regulators of carpel suppression, we performed a gt1 enhancer screen and found a genetic interaction between gt1 and ramosa3 (ra3). RA3 is a classic inflorescence meristem determinacy gene that encodes a trehalose-6-phosphate (T6P) phosphatase (TPP). Dissection of floral development revealed that ra3 single mutants have partially derepressed carpels, whereas gt1;ra3 double mutants have completely derepressed carpels. Surprisingly, gt1 suppresses ra3 inflorescence branching, revealing a role for gt1 in meristem determinacy. Supporting these genetic interactions, GT1 and RA3 proteins colocalize to carpel nuclei in developing flowers. Global expression profiling revealed common genes misregulated in single and double mutant flowers, as well as in derepressed gt1 axillary meristems. Indeed, we found that ra3 enhances gt1 vegetative branching, similar to the roles for the trehalose pathway and GT1 homologs in the eudicots. This functional conservation over ∼160 million years of evolution reveals ancient roles for GT1-like genes and the trehalose pathway in regulating axillary meristem suppression, later recruited to mediate carpel suppression. Our findings expose hidden pleiotropy of classic maize genes and show how an ancient developmental program was redeployed to sculpt floral form.

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Section: Discussionmentioning

confidence: 99%

Recruitment of an ancient branching program to suppress carpel development in maize flowers

Klein

Gallagher

Demesa-Arévalo

et al. 2022

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

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“…Targeted mutagenesis via ‘genome editing’ by means of customizable endonucleases is a new breeding technology that can efficiently produce desired mutants in a target gene and has been applied to generate mutants in multiple crop species, including barley (Gerasimova et al ., 2020 ; Kapusi et al ., 2017 ; Lawrenson et al ., 2015 ; Thiel et al ., 2021 ). Genome editing makes it possible to create single or multiple mutations at the target site(s) of choice without any alteration in the genetic background, allowing for powerful analyses of the effects of individual genes and their genetic interactions.…”

Section: Introductionmentioning

confidence: 99%

Regulation of germination by targeted mutagenesis of grain dormancy genes in barley

Hisano

Hoffie

Abe

et al. 2021

Plant Biotechnology Journal

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Summary High humidity during harvest season often causes pre‐harvest sprouting in barley (Hordeum vulgare). Prolonged grain dormancy prevents pre‐harvest sprouting; however, extended dormancy can interfere with malt production and uniform germination upon sowing. In this study, we used Cas9‐induced targeted mutagenesis to create single and double mutants in QTL FOR SEED DORMANCY 1 (Qsd1) and Qsd2 in the same genetic background. We performed germination assays in independent qsd1 and qsd2 single mutants, as well as in two double mutants, which revealed a strong repression of germination in the mutants. These results demonstrated that normal early grain germination requires both Qsd1 and Qsd2 function. However, germination of qsd1 was promoted by treatment with 3% hydrogen peroxide, supporting the notion that the mutants exhibit delayed germination. Likewise, exposure to cold temperatures largely alleviated the block of germination in the single and double mutants. Notably, qsd1 mutants partially suppress the long dormancy phenotype of qsd2, while qsd2 mutant grains failed to germinate in the light, but not in the dark. Consistent with the delay in germination, abscisic acid accumulated in all mutants relative to the wild type, but abscisic acid levels cannot maintain long‐term dormancy and only delay germination. Elucidation of mutant allele interactions, such as those shown in this study, are important for fine‐tuning traits that will lead to the design of grain dormancy through combinations of mutant alleles. Thus, these mutants will provide the necessary germplasm to study grain dormancy and germination in barley.

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“…HvTCP2 is highly expressed in the shoot apex, but follows an opposite trend in time when compared to VRS5 and HvTB2. Recently, it was shown that VRS5 is higher expressed in the lateral spikelet when compared to the central spikelets (Thiel et al 2021). A more closer look at the HvTB2 expression suggests that this gene is highly expressed in both the central and the lateral spikelets within the developing shoot apex (Supplementary Fig.…”

Section: Vrs5 Forms Heterodimers With Closely Related Class II Tcp Tfmentioning

confidence: 90%

“…Overall, TCPs were expressed in various tissue types and developmental stages (Supplementary Fig. 1) (Thiel et al 2021). Barley TCPs have a close phylogenetic relationship to hexaploid wheat, which contains three copies of each TCP on the A, B and D genomes.…”

Section: Barley Class II Tcps Have a Grass-specific Sister Clade Of Tb1mentioning

confidence: 99%

“…For biological relevance, genes encoding interacting proteins should be co-expressed and therefore, we compared the expression patterns and levels of VRS5 and of the genes encoding the interacting TCP TF in the developing shoot apex, extracted from available RNA-Seq data of cv Bowman apical meristems (van Esse et al 2017;Walla et al 2020;Thiel et al 2021). Both VRS5 and HvTB2 have a low expression at the double ridge stage, their expression increases in the lemma and stamen primordia stages (LP/SP) and is highest in the awn primordia stage (AP) (Fig.…”

Section: Vrs5 Forms Heterodimers With Closely Related Class II Tcp Tfmentioning

confidence: 99%

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The TCP transcription factor HvTB2 heterodimerizes with VRS5 and controls spike architecture in barley

Moraes

Hernández-Pinzón

et al. 2022

Plant Reprod

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Key message Understanding the molecular network, including protein-protein interactions, of VRS5 provide new routes towards the identification of other key regulators of plant architecture in barley. Abstract The TCP transcriptional regulator TEOSINTE BRANCHED 1 (TB1) is a key regulator of plant architecture. In barley, an important cereal crop, HvTB1 (also referred to as VULGARE SIX-ROWED spike (VRS) 5), inhibits the outgrowth of side shoots, or tillers, and grains. Despite its key role in barley development, there is limited knowledge on the molecular network that is utilized by VRS5. In this work, we performed protein–protein interaction studies of VRS5. Our analysis shows that VRS5 potentially interacts with a diverse set of proteins, including other class II TCP’s, NF-Y TF, but also chromatin remodelers. Zooming in on the interaction capacity of VRS5 with other TCP TFs shows that VRS5 preferably interacts with other class II TCP TFs in the TB1 clade. Induced mutagenesis through CRISPR–Cas of one of the putative VRS5 interactors, HvTB2 (also referred to as COMPOSITUM 1 and BRANCHED AND INDETERMINATE SPIKELET 1), resulted in plants that have lost their characteristic unbranched spike architecture. More specifically, hvtb2 mutants exhibited branches arising at the main spike, suggesting that HvTB2 acts as inhibitor of branching. Our protein–protein interaction studies of VRS5 resulted in the identification of HvTB2 as putative interactor of VRS5, another key regulator of spike architecture in barley. The study presented here provides a first step to underpin the protein–protein interactome of VRS5 and to identify other, yet unknown, key regulators of barley plant architecture.

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Transcriptional landscapes of floral meristems in barley

Cited by 36 publications

References 98 publications

Recruitment of an ancient branching program to suppress carpel development in maize flowers

Recruitment of an ancient branching program to suppress carpel development in maize flowers

Regulation of germination by targeted mutagenesis of grain dormancy genes in barley

The TCP transcription factor HvTB2 heterodimerizes with VRS5 and controls spike architecture in barley

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