Biosynthesis of riccionidins and marchantins is regulated by R2R3-MYB transcription factors in Marchantia polymorpha

Kubo, Hisahiko; Nozawa, Shiro; Hiwatashi, Takuma; Kondou, Youichi; Nakabayashi, Ryo; Mori, Tetsuya; Saito, Kazuki; Takanashi, Kojiro; Kohchi, Takayuki; Ishizaki, Kimitsune

doi:10.1007/s10265-018-1044-7

Cited by 54 publications

(81 citation statements)

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“…In addition, three TF genes ( Mp3g07510 , Mp MYB02; Mp5g01530 , Mp NAC06 and Mp2g16340 , Mp Trihelix28 ) are down-regulated (Figure 5A). Mp MYB02 is known to regulate cyclic bis(bibenzyl) acids biosynthesis [35] which accumulates in oil bodies [15]. The mutant also exhibited significantly reduced expression of Mp SYP12B ( Mp4g20670 ), a N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) protein with specific localization at the oil body membrane of M. polymorpha [60].…”

Section: Resultsmentioning

confidence: 99%

“…As oil bodies form at low frequency in Mp c1hdz mutants, other transcriptional regulators could be important for oil body cell differentiation. The R2R3-MYB TFs Mp MYB02 and Mp MYB14 control the bis(bibenzyl) and auronidin biosynthesis, respectively [35, 37]. Mp c1hdz mutants showed a strong repression of Mp MYB02 expression, whereas Mp MYB14 , important for the defense against the oomycete pathogen Phytophthora palmivora [71], remained unchanged (Table S1, S2).…”

Section: Discussionmentioning

confidence: 99%

“…Mp c1hdz mutants showed a strong repression of Mp MYB02 expression, whereas Mp MYB14 , important for the defense against the oomycete pathogen Phytophthora palmivora [71], remained unchanged (Table S1, S2). That Mp C1HDZ expression is not altered in Mp MYB02 gain-of-function alleles [35] suggests that Mp MYB02 is downstream MpC1HDZ activity, however, it is unknown whether MpMYB02 is also specifically expressed in oil body cells or participates in oil body cell differentiation and terpenoid biosynthesis. In contrast, we did not find any relationship of Mp C1HDZ with Mp MYCX/Y , which is associated with the defense-related induction of sesquiterpenoid biosynthesis in response to herbivory [67], or with ABA signaling, which is associated with bis(bibenzyl) increase under UV-C light stress [38].…”

Section: Discussionmentioning

confidence: 99%

“…Synthesis of specialized metabolites in vascular plants is tightly regulated by transcription factors (TFs), with some orthologs having conserved and others novel roles in liverworts [32, 35-38]. Class I HOMEODOMAIN LEUCINE-ZIPPER (C1HDZ) TFs genes are conserved across streptophytes with a single homolog predicted to have been present in the common-ancestor of land plants [39].…”

Section: Introductionmentioning

confidence: 99%

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Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

Romani

Banić

Florent

et al. 2020

Preprint

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26 27 28 SUMMARY 29 The origin of a terrestrial flora in the Ordovician required adaptation to novel biotic and abiotic 30 stressors. Oil bodies, a synapomorphy of liverworts, accumulate secondary metabolites, but their 31 function and development are poorly understood. Oil bodies of Marchantia polymorpha develop 32 within specialized cells as one single large organelle. Here, we show that a CLASS I 33 HOMEODOMAIN LEUCINE-ZIPPER (C1HDZ) transcription factor controls the differentiation of 34 oil body cells in two different ecotypes of the liverwort M. polymorpha, a model genetic system for 35 early divergent land plants. In flowering plants, these transcription factors primarily modulate 36 responses to abiotic stresss including drought. However, loss-of-function alleles of the single ortholog 37 gene, MpC1HDZ, in M. polymorpha did not exhibit phenotypes associated with abiotic stress. Rather 38 Mpc1hdz mutant plants were more susceptible to herbivory and total plant extracts of the mutant 39 exhibited reduced antibacterial activity. Transcriptomic analysis of the mutant revealed a reduction 40 in expression of genes related to secondary metabolism that was accompanied by a specific depletion 41 of oil body terpenoid compounds. Through time lapse imaging we observed that MpC1HDZ 42 expression maxima precede oil body formation indicating that MpC1HDZ mediates differentiation 43 of oil body cells. Our results indicate that M. polymorpha oil bodies, and MpC1HDZ, are critical for 44 defense against herbivory but not for abiotic stress-tolerance. Thus, C1HDZ genes were co-opted to 45 regulate separate responses to biotic and abiotic stressors in two distinct land plant lineages.46 47 48 49 The emergence of land flora in the Ordovician and the subsequent radiation of plants into terrestrial 50 environments were major evolutionary events in the history of Earth. This radical breakthrough for 51 life on the planet entailed the evolution of both new developmental programs and biochemical 52 pathways [1]. Early land plants were faced with novel biotic and abiotic stressors, including a 53 desiccating aerial environment, increased solar radiation, and greater interspecific competition, 54 including herbivory. This transition was accompanied by a dramatic increase in the diversity of 55 secondary metabolites and the complexity of transcriptional regulation, to protect plants from 56 herbivores and pathogens, and also abiotic stressors such as desiccation and light intensity [2-4]. 57 Liverworts represent one of the earliest diverging land plant lineages, with a predicted Ordovician-58 Silurian origin of all three major extant liverwort clades [5, 6]. One synapomorphy of this lineage is 59 the presence of oil bodies, specialized organelles containing an array of lipophilic secondary 60 compounds [7]. In some liverworts, multiple oil bodies are found in nearly all differentiated cells of 61 both gametophyte and sporophyte generations. Whilst in other liverworts, such as Marchantia 62 polymorpha (M. polymorpha), oil bodies are ...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

Romani

Banić

Florent

et al. 2020

Preprint

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“…4h). MpMYB02, whose expression was also positively regulated by MpERF13, is reported to be a transcription factor responsible for the production of marchantin A and its derivatives that accumulate in oil bodies 9, 26 . Mp ABCG1 and Mp MYB02 are specifically expressed in oil body cells and when sec-mRFP was driven by the promoters of these genes, it was specifically targeted to the lumen of oil bodies.…”

Section: Main Textmentioning

confidence: 99%

Switching secretory pathway direction for organelle acquisition in plants

Kanazawa

Morinaka

Ebine

et al. 2020

Preprint

Self Cite

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26Eukaryotic cells acquired novel organelles during evolution through mechanisms that 27 remain largely obscure. The existence of the unique oil body compartment is a 28 synapomorphy of liverworts that represents lineage-specific acquisition of this organelle 29 during evolution, although its origin, biogenesis, and physiological function are yet 30 unknown. We found that two Syntaxin 1 paralogs in the liverwort, Marchantia 31 polymorpha, are distinctly targeted to forming cell plates and the oil body, suggesting 32 these structures share some developmental similarity. Oil body formation is under the 33 regulation of an ERF/AP2-type transcription factor and loss of the oil body increased M. 34 polymorpha herbivory. These findings highlight a common strategy for the acquisition 35 of organelles with distinct functions in plants, via periodical switching in secretion 36 direction depending on cellular phase transition. 37 38 Main text: 39 Eukaryotic cells originated from prokaryotes by expanding their 40 endomembrane network during evolution, with the last eukaryotic common 41 ancestor (LECA) likely possessing a complex set of organelles 1 . New membrane 42 trafficking pathways were added to the LECA endomembrane network, some of 43 which were secondarily lost in a lineage-specific manner, resulting in divergent 44 and organism-specific membrane trafficking systems and organelle compositions 45 of extant eukaryotes 2-4 . It remains mostly unknown how organelles were acquired 46during evolution. We report that the liverwort-specific oil body was acquired by 47

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Conservation and Divergence Between Bryophytes and Angiosperms in the Biosynthesis and Regulation of Flavonoid Production

Davies

Jibran

Albert

et al. 2021

Recent Advances in Polyphenol Research

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Biosynthesis of riccionidins and marchantins is regulated by R2R3-MYB transcription factors in Marchantia polymorpha

Cited by 54 publications

References 79 publications

Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

Switching secretory pathway direction for organelle acquisition in plants

Conservation and Divergence Between Bryophytes and Angiosperms in the Biosynthesis and Regulation of Flavonoid Production

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