Tomato<i>HAIRY MERISTEM</i>genes are involved in meristem maintenance and compound leaf morphogenesis

Hendelman, Anat; Kravchik, Michael; Stav, Ran; Frank, Wolfgang; Arazi, Tzahi

doi:10.1093/jxb/erw388

Cited by 25 publications

(28 citation statements)

References 38 publications

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“…SEM analysis of wild‐type and CR‐slmir160a reproductive organs were prepared as described previously (Hendelman et al ., ) and viewed in a Jeol 5410 LV microscope (Jeol, https://www.jeol.co.jp/). For SEM analysis of CR‐slmir160a shoot apices and CR‐slarf10a‐9 pistils, plant fresh tissues were collected and immediately characterized using TM3030Plus Tabletop Microscope (Hitachi, http://www.hitachi.com/).…”

Section: Methodsmentioning

confidence: 99%

“…The binary constructs pRCS-35S:Cas9-U6:SlMIR160b, pRCS-35S: Cas9-U6:SlMIR160a, pRCS-35S:Cas9-U6:SlARF10A/16A/17, and pART27-35S:MIR160a were transformed into tomato cv. M82 as described in Damodharan et al, 2016. Histological analysis and microscopy SEM analysis of wild-type and CR-slmir160a reproductive organs were prepared as described previously (Hendelman et al, 2016) and viewed in a Jeol 5410 LV microscope (Jeol, https://www.jeol.c o.jp/). For SEM analysis of CR-slmir160a shoot apices and CR-slarf10a-9 pistils, plant fresh tissues were collected and immediately characterized using TM3030Plus Tabletop Microscope (Hitachi, http://www.hitachi.com/).…”

Section: Tomato Transformationmentioning

confidence: 99%

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Tuning of SlARF10A dosage by sly‐miR160a is critical for auxin‐mediated compound leaf and flower development

et al. 2018

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miR160 adjusts auxin-mediated development by post-transcriptional regulation of the auxin response factors ARF10/16/17. In tomato, knockdown of miR160 (sly-miR160) suggested that it is required for auxin-driven leaf blade outgrowth, but whether additional developmental events are adjusted by sly-miR160 is not clear. Here, the SlMIR160 genes and the genes of its SlARFs targets were edited by CRISPR/Cas9 resulting in the isolation of loss-of-function mutants. In addition, hypomorphic mutants that accumulate variable reduced levels of sly-miR160a were isolated. We found that the loss-of-function mutants in SlMIR160a (CR-slmir160a-6/7) produced only four wiry leaves, whereas the hypomorphic mutants developed leaves and flowers with graded developmental abnormalities. Phenotypic severity correlated with the upregulation of SlARF10A. Consistent with that, double mutants in SlMIR160a and SlARF10A restored leaf and flower development indicating that over-accumulation of SlARF10A underlay the developmental abnormalities exhibited in the CR-slmir160a mutants. Phenotype severity also correlated with the upregulation of the SHOOT MERISTEMLESS homolog Tomato Knotted 2, which in turn activated the transcription of the cytokinin biosynthesis genes SlIPT2 and SlIPT4. However, no change in Tomato Knotted 2 was detected in the absence of SlARF10A, suggesting that it is upregulated due to auxin signaling suppression by SlARF10A. Knockout of sly-miR160a-targeted SlARFs showed that whereas SlARF10A is indispensable for leaf blade outgrowth and floral organ patterning, the functions of SlARF16A and SlARF17 are redundant. Taken together our results suggest that sly-miR160a promotes blade outgrowth as well as leaf and leaflet initiation and floral organ development through the quantitative regulation of its major target SlARF10A.

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Section: Methodsmentioning

confidence: 99%

Section: Tomato Transformationmentioning

confidence: 99%

Tuning of SlARF10A dosage by sly‐miR160a is critical for auxin‐mediated compound leaf and flower development

et al. 2018

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“…Members of a miR171 family contain one or more nucleotide changes similar to members from other miRNA families, but unlike other conserved miRNAs they may be offset by three nucleotides relative to each other [5]. This atypical sequence offset may result in different target specificities for certain miR171 members [6]. Hitherto, miR171 members have been demonstrated to guide the cleavage of mRNAs coding for GRAS domain SCARECROW-like transcription factors that belong to the HAIRY MERISTEM (HAM) or NODULATION SIGNALING PATHWAY (NSP) clades [6,7,8].…”

Section: Introductionmentioning

confidence: 99%

“…This atypical sequence offset may result in different target specificities for certain miR171 members [6]. Hitherto, miR171 members have been demonstrated to guide the cleavage of mRNAs coding for GRAS domain SCARECROW-like transcription factors that belong to the HAIRY MERISTEM (HAM) or NODULATION SIGNALING PATHWAY (NSP) clades [6,7,8].…”

Section: Introductionmentioning

confidence: 99%

“…Previously, we have demonstrated that sly-miR171a and sly-miR171b guide the cleavage of SlHAM and SlHAM2 and sly-miR171b also guides the cleavage of the tomato NSP2 homolog SlNSP2L . Sly-miR171a and sly-miR171b overexpression resulted in over-proliferation of meristematic cells in the periphery of meristems and in the organogenic compound leaf rachis, suggesting that sly-miR171-targeted SlHAMs function in meristem maintenance and compound leaf morphogenesis [6]. As part of our continuous effort to unravel the identity and roles of tomato miRNAs, in the current study, we re-annotated the tomato miR171 family and utilized the STTM approach to silence abundant members in the family and investigate their functions.…”

Section: Introductionmentioning

confidence: 99%

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Functional Characterization of microRNA171 Family in Tomato

Kravchik

Stav

Belausov

et al. 2019

Plants

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Deeply conserved plant microRNAs (miRNAs) function as pivotal regulators of development. Nevertheless, in the model crop Solanum lycopersicum (tomato) several conserved miRNAs are still poorly annotated and knowledge about their functions is lacking. Here, the tomato miR171 family was functionally analyzed. We found that the tomato genome contains at least 11 SlMIR171 genes that are differentially expressed along tomato development. Downregulation of sly-miR171 in tomato was successfully achieved by transgenic expression of a short tandem target mimic construct (STTM171). Consequently, sly-miR171-targeted mRNAs were upregulated in the silenced plants. Target upregulation was associated with irregular compound leaf development and an increase in the number of axillary branches. A prominent phenotype of STTM171 expressing plants was their male sterility due to a production of a low number of malformed and nonviable pollen. We showed that sly-miR171 was expressed in anthers along microsporogenesis and significantly silenced upon STTM171 expression. Sly-miR171-silenced anthers showed delayed tapetum ontogenesis and reduced callose deposition around the tetrads, both of which together or separately can impair pollen development. Collectively, our results show that sly-miR171 is involved in the regulation of anther development as well as shoot branching and compound leaf morphogenesis.

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PpGRAS12 acts as a positive regulator of meristem formation in Physcomitrium patens

et al. 2021

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Key message This study focused on the key regulatory function of Physcomitrium patens GRAS12 gene underlying an increasing plant complexity, an important step in plant terrestrialization and the evolutionary history of life. Abstract The miR171‐GRAS module has been identified as a key player in meristem maintenance in angiosperms. PpGRAS12 is a member of the GRAS family and a validated target for miR171 in Physcomitrium (Physcomitrella) patens. Here we show a regulatory function of miR171 at the gametophytic vegetative growth stage and targeted deletion of the PpGRAS12 gene adversely affects sporophyte production since fewer sporophytes were produced in ΔPpGRAS12 knockout lines compared to wild type moss. Furthermore, highly specific and distinct growth arrests were observed in inducible PpGRAS12 overexpression lines at the protonema stage. Prominent phenotypic aberrations including the formation of multiple apical meristems at the gametophytic vegetative stage in response to elevated PpGRAS12 transcript levels were discovered via scanning electron microscopy. The production of multiple buds in the PpGRAS12 overexpression lines similar to ΔPpCLV1a/1b disruption mutants is accompanied by an upregulation of PpCLE and downregulation of PpCLV1, PpAPB, PpNOG1, PpDEK1, PpRPK2 suggesting that PpGRAS12 acts upstream of these genes and negatively regulates the proposed pathway to specify simplex meristem formation. As CLV signaling pathway components are not present in the chlorophytic or charophytic algae and arose with the earliest land plants, we identified a key regulatory function of PpGRAS12 underlying an increasing plant complexity, an important step in plant terrestrialization and the evolutionary history of life.

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TomatoHAIRY MERISTEMgenes are involved in meristem maintenance and compound leaf morphogenesis

Abstract: HighlightFunctional analysis of the tomato HAM genes suggest that they are involved in critical meristem functions and play homologous roles in compound leaf development.

Cited by 25 publications

References 38 publications

Tuning of SlARF10A dosage by sly‐miR160a is critical for auxin‐mediated compound leaf and flower development

Tuning of SlARF10A dosage by sly‐miR160a is critical for auxin‐mediated compound leaf and flower development

Functional Characterization of microRNA171 Family in Tomato

PpGRAS12 acts as a positive regulator of meristem formation in Physcomitrium patens

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