Triterpenoids in aerenchymatous phellem contribute to internal root aeration and waterlogging adaptability in soybean

Takahashi, Hirokazu; Abo, Chisato; Suzuki, Hayato; Romsuk, Jutapat; Oi, Takao; Yanagawa, Asako; Gorai, Tomoka; Tomisaki, Yukari; Jitsui, Mana; Shimamura, Satoshi; Mori, Hitoshi; Kaga, Akito; Ishimoto, Masao; Seki, Hikaru; Muranaka, Toshiya; Nakazono, Mikio

doi:10.21203/rs.3.rs-2230730/v1

Cited by 5 publications

(5 citation statements)

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“…The triterpenoid profiles of LORE1 insertion mutant lines of L. japonicus accession Gifu B-129 ( Fukai et al., 2012 ; Urbański et al., 2012 ) were analyzed to investigate the effect of loss-of-function of either LjCPR1 or LjCPR2 genes. Based on a previous study, LUS and CYP716A s genes that are responsible for lupeol and betulinic acid production, respectively, were upregulated in secondary aerenchyma of hydroponic-cultured L. japonicus ( Suzuki et al., 2022 ) and soybean plants under flooded conditions ( Takahashi et al., 2022 ). Therefore, to investigate if plant culture condition affects LjCPRs’ involvement with specific CYPs, the Ljcpr1 and Ljcpr2-1 loss-of-function mutant lines were both cultured in soil and a hydroponic system.…”

Section: Resultsmentioning

confidence: 99%

Class I and II NADPH-cytochrome P450 reductases exhibit different roles in triterpenoid biosynthesis in Lotus japonicus

et al. 2023

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Cytochrome P450 monooxygenases (CYPs) are enzymes that play critical roles in the structural diversification of triterpenoids. To perform site-specific oxidations of the triterpene scaffold, CYPs require electrons transferred by NADPH-cytochrome P450 reductase (CPR), which is classified into two main classes, class I and class II, based on their structural difference. Lotus japonicus is a triterpenoids-producing model legume with one CPR class I gene (LjCPR1) and a minimum of two CPR class II genes (LjCPR2-1 and LjCPR2-2). CPR classes I and II from different plants have been reported to be involved in different metabolic pathways. By performing gene expression analyses of L. japonicus hairy root culture treated with methyl jasmonate (MeJA), this study revealed that LjCPR1, CYP716A51, and LUS were down-regulated which resulted in no change in betulinic acid and lupeol content. In contrast, LjCPR2s, bAS, CYP93E1, and CYP72A61 were significantly upregulated by MeJA treatment, followed by a significant increase of the precursors for soyasaponins, i.e. β-amyrin, 24-OH β-amyrin, and sophoradiol content. Triterpenoids profile analysis of LORE1 insertion and hairy root mutants showed that the loss of the Ljcpr2-1 gene significantly reduced soyasaponins precursors but not in Ljcpr1 mutants. However, Ljcpr1 and Ljcpr2-1 mutants showed a significant reduction in lupeol and oleanolic, ursolic, and betulinic acid contents. Furthermore, LjCPR1, but not LjCPR2, was crucial for seed development, supporting the previous notion that CPR class I might support plant basal metabolism. This study suggests that CPR classes I and II play different roles in L. japonicus triterpenoid biosynthesis.

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Section: Resultsmentioning

confidence: 99%

Class I and II NADPH-cytochrome P450 reductases exhibit different roles in triterpenoid biosynthesis in Lotus japonicus

et al. 2023

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“…The role of aerenchyma, including SA, is to supply air to roots under flooded conditions (Colmer & Pedersen, 2008; Shimamura et al ., 2010; Takahashi et al ., 2014). Our recent study revealed that G. max also accumulated BA in SA under flooded conditions and suggested that the accumulation of hydrophobic BA was essential to exclude water from gas spaces and promote air diffusion (Takahashi et al 2022).…”

Section: Discussionmentioning

confidence: 99%

Identification of basic helix-loop-helix transcription factors that activate betulinic acid biosynthesis by RNA-sequencing of hydroponically culturedLotus japonicus

Suzuki

Takahashi

Fukushima

et al. 2022

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Although triterpenes are ubiquitous in plant kingdom, their biosynthetic regulatory mechanisms are limitedly understood. Here, we found that hydroponic culture dramatically activated betulinic acid (BA) biosynthesis in the model FabaceaeLotus japonicus, and investigated its transcriptional regulation. Fabaceae plants develop secondary aerenchyma (SA) on the surface of hypocotyls and roots during flooding for root air diffusion. Hydroponic culture induced SA inL. japonicusand simultaneously increased the accumulation of BA and the transcript levels of its biosynthetic genes. RNA-sequencing of soil-grown and hydroponically cultured plant tissues, including SA collected by laser microdissection, revealed that several transcription factor genes were co-upregulated with BA biosynthetic genes. Overexpression ofLjbHLH32andLjbHLH50inL. japonicustransgenic hairy roots upregulated the expression of BA biosynthesis genes, resulting in enhanced BA accumulation. However, transient luciferase reporter assays inArabidopsismesophyll cell protoplasts showed that LjbHLH32 transactivated promoters of biosynthetic genes in the soyasaponin pathway but not the BA pathway, like its homolog GubHLH3, a soyasaponin biosynthesis regulator inGlycyrrhiza uralensis. This suggested the evolutionary origin and complex regulatory mechanisms of BA biosynthesis in Fabaceae. This study sheds light on the unrevealed biosynthetic regulatory mechanisms of triterpenes in Fabaceae plants.

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“…The triterpenoid profiles of LORE1 insertion mutant lines of L. japonicus accession Gifu B-129 (Fukai et al, 2012;Urbański et al, 2012) were analyzed to investigate the effect of loss-of-function of either LjCPR1 or LjCPR2 genes. Based on a previous study, LUS and CYP716As genes that are responsible for lupeol and betulinic acid production, respectively, were upregulated in secondary aerenchyma of hydroponic-cultured L. japonicus (Suzuki et al, 2022) and soybean plants under flooded conditions (Takahashi et al, 2022). Therefore, to investigate if plant culture condition affects LjCPRs' involvement with specific CYPs, the Ljcpr1 and Ljcpr2-1 loss-of-function mutant lines were both cultured in soil and a hydroponic system.…”

Section: Ljcpr1 and Ljcpr2-1 Loss-of-function Mutant Plantsmentioning

confidence: 99%

Advances in Discoveries of Plant Phytochemicals

2024

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Triterpenoids in aerenchymatous phellem contribute to internal root aeration and waterlogging adaptability in soybean

Cited by 5 publications

References 44 publications

Class I and II NADPH-cytochrome P450 reductases exhibit different roles in triterpenoid biosynthesis in Lotus japonicus

Class I and II NADPH-cytochrome P450 reductases exhibit different roles in triterpenoid biosynthesis in Lotus japonicus

Identification of basic helix-loop-helix transcription factors that activate betulinic acid biosynthesis by RNA-sequencing of hydroponically culturedLotus japonicus

Advances in Discoveries of Plant Phytochemicals

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