The phosphorylated pathway of serine biosynthesis links plant growth with nitrogen metabolism

Zimmermann, Sandra; Benstein, Ruben Maximilian; Flores-Tornero, María; Blau, Samira; Anoman, Armand D.; Rosa-Téllez, Sara; Gerlich, Silke C.; Salem, Mohamed A.; Alseekh, Saleh; Wewer, Vera; Flügge, Ulf‐Ingo; Jacoby, Richard P.; Fernie, Alisdair R.; Giavalisco, Patrick; Ros, Roc; Krueger, Stephan

doi:10.1093/plphys/kiab167

Cited by 35 publications

(98 citation statements)

References 85 publications

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“…They may also play an important role in DA biosynthesis. PGDH was involved in the biosynthesis of serine [ 37 ], which provides the N source for atisine-type C 20 -DAs [ 38 ]. Additionally, the transcription factor TIFY (transcript 65043) showed a suitable correlation with TIFY (transcript 72154), CYP450 (transcript 36192), 2-ODD (transcript 59503), and BAHD-type acyltransferase (transcript 50810, transcript 49129).…”

Section: Resultsmentioning

confidence: 99%

Integrating Metabolomics and Transcriptomics to Unveil Atisine Biosynthesis in Aconitum gymnandrum Maxim

Chen

Tian

Jin

et al. 2022

IJMS

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Diterpene alkaloids (DAs) are characteristic compounds in Aconitum, which are classified into four skeletal types: C18, C19, C20, and bisditerpenoid alkaloids. C20-DAs are thought to be the precursor of the other types. Their biosynthetic pathway, however, is largely unclear. Herein, we combine metabolomics and transcriptomics to unveil the methyl jasmonate (MJ) inducible biosynthesis of DAs in the sterile seedling of A. gymnandrum, the only species in the Subgenus Gymnaconitum (Stapf) Rapaics. Target metabolomics based on root and aerial portions identified 51 C19-DAs and 15 C20-DAs, with 40 inducible compounds. The highest content of C20-DA atisine was selected for further network analysis. PacBio Isoform sequencing integrated with RNA sequencing not only provided the full-length transcriptome but also their response to induction, revealing 1994 genes that exhibited up-regulated expression. Further, 38 genes involved in terpenoid biosynthesis were identified, including 7 diterpene synthases. In addition to the expected function of the four diterpene synthases, AgCPS5 was identified to be a new ent-8,13-CPP synthase in Aconitum and could also combine with AgKSL1 to form the C20-DAs precursor ent-atiserene. Combined with multiple network analyses, six CYP450 and seven 2-ODD genes predicted to be involved in the biosynthesis of atisine were also identified. This study not only sheds light on diterpene synthase evolution in Aconitum but also provides a rich dataset of full-length transcriptomes, systemic metabolomes, and gene expression profiles, setting the groundwork for further investigation of the C20-DAs biosynthesis pathway.

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Section: Resultsmentioning

confidence: 99%

Integrating Metabolomics and Transcriptomics to Unveil Atisine Biosynthesis in Aconitum gymnandrum Maxim

Chen

Tian

Jin

et al. 2022

IJMS

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“…We remained puzzled by the bias towards enhanced nitrogenous compounds in pdx3 and strived to define which cellular functions were perturbed by the lack of PDX3 activity. Recently, the phosphorylated pathway of serine biosynthesis (PPSB) has been shown to be vital for Arabidopsis plant growth (Zimmermann et al, 2021). The PPSB pathway is predominantly active in plant roots and is a major contributor to the serine pool, especially under elevated CO 2 , when photorespiration is repressed (Zimmermann et al, 2021).…”

Section: Resultsmentioning

confidence: 99%

“…This notion was supported by the fact that 3-phosphoserine aminotransferase (PSAT), an enzyme of the PPSB pathway, is dependent on PLP for activity (Wulfert and Krueger, 2018). As external feeding with serine has been shown to be metabolized the same way as the plant would by biosynthesis de novo (Zimmermann et al, 2021), we tested if serine supplementation could improve growth of pdx3 plants under elevated CO 2 . Indeed, growth of pdx3 on culture plates under elevated CO 2 was considerably improved in the presence of serine (Figure 4C).…”

Section: Resultsmentioning

confidence: 99%

“…Surprisingly, exploration of photorespiration as a source of endogenous N driving this metabolic imbalance, by incubation under high CO 2 , further exacerbated the pdx3 growth phenotype. Interestingly, the amino acid serine, which is critical for growth and N management (Zimmermann et al, 2021), alleviates the growth phenotype of pdx3 plants under high CO 2 . Triggering of thermomorphogenesis by growth of plants at 28°C (instead of 22°C) is another condition that does not appear to require PDX3 function, and we observed that the consequent drive towards C metabolism counters the c/N imbalance in pdx3 .…”

Section: Introductionmentioning

confidence: 99%

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PDX3 is important for carbon/nitrogen balance in Arabidopsis associated with distinct environmental conditions

Steensma

Eisenhut

Colinas

et al. 2022

Preprint

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To survive and proliferate in diverse environments with varying climate and nutrient availability, plants modulate their metabolism. Achieving a balance between carbon (C) and nitrogen (N) use such that growth and defense mechanisms can be appropriately controlled is critical for plant fitness. The identification of factors that regulate C/N utilization in plants can make a significant contribution to optimization of plant health. Here we show that pyridox(am)ine 5'-phosphate oxidase (PDX3), which regulates vitamin B6 homeostasis, influences C/N balance. The B6 vitamer imbalance resulting from loss of PDX3 leads to over-accumulation of nitrogenous compounds. A combination of increased glutamate dehydrogenase activity, impairment in the photorespiratory cycle and inappropriate use of endogenous ammonium fuel the metabolic imbalance. Growth at elevated CO2 levels further exacerbates the pdx3 phenotypes. Interestingly, serine supplementation rescues growth under high CO2 likely bypassing the phosphorylated pathway of biosynthesis suggesting that this amino acid is an important commodity. We show that PDX3 function appears dispensable upon thermomorphogenesis, a condition that favors C metabolism. Furthermore, while a low ammonium to nitrate ratio likely accounts for overstimulation of salicylic acid (SA) defense responses in pdx3 lines that compromises growth, a basal level of SA protects against loss of PDX3 biochemical function. Overall, the study highlights environmental scenarios where vitamin B6 homeostasis, as managed by the salvage pathway enzyme PDX3, is critical and provides insight into how plants reprogram their metabolism under such conditions.

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“…Plants with reduced PPSB activity tend to exhibit a strong shoot and root growth retardation phenotype, or a lethal phenotype due to disturbed male gametophyte and embryo development. Plastid glycolysis provides the 3-PGA for PPSB, and defective PPSB can disrupt the entire carbon metabolism in plants [ 21 ]. PPSB can provide 2-oxoglutarate for glutamate synthesis and subsequent ammonium fixation (by the GS/GOGAT cycle), as well as participating in the TCA cycle through 2-oxoglutarate [ 22 ].…”

Section: Introductionmentioning

confidence: 99%

Over-Expression of Phosphoserine Aminotransferase-Encoding Gene (AtPSAT1) Prompts Starch Accumulation in L. turionifera under Nitrogen Starvation

Wang

Sun

et al. 2022

IJMS

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It has been demonstrated that the phosphorylation pathway of L-serine (Ser) biosynthesis (PPSB) is very important in plant growth and development, but whether and how PPSB affects nitrogen metabolism and starch accumulation has not been fully elucidated. In this study, we took the energy plant duckweed (strain Lemna turionifera 5511) as the research object and used a stable genetic transformation system to heterologously over-expressing Arabidopsis AtPSAT1 (the gene encoding phosphoserine aminotransferase, the second enzyme of PPSB). Our results showed that, under nitrogen starvation, the transgenic plants grew faster, with higher values of Fv/Fm, rETR, and Y(II), as well as fresh and dry weight, than the wild-type. More promisingly, the accumulation of starch was also found to be significantly improved when over-expressing AtPSAT1 in the transgenic plants. qRT-PCR analysis results showed that the expression of genes related to nitrogen assimilation, carbon metabolism, and starch biosynthesis was up-regulated, while the expression of starch degradation-related genes was down-regulated by AtPSAT1 over-expression. We propose that the increased starch accumulation caused by AtPSAT1 over-expression may result from both elevated photosynthetic capacity and nitrogen utilization efficiency. This research sheds new light on the mechanism underlying the ability of PPSB to coordinate nitrogen and carbon metabolism, and provides a feasible way to improve starch production, that is, through engineering PPSB in crops.

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The phosphorylated pathway of serine biosynthesis links plant growth with nitrogen metabolism

Cited by 35 publications

References 85 publications

Integrating Metabolomics and Transcriptomics to Unveil Atisine Biosynthesis in Aconitum gymnandrum Maxim

Integrating Metabolomics and Transcriptomics to Unveil Atisine Biosynthesis in Aconitum gymnandrum Maxim

PDX3 is important for carbon/nitrogen balance in Arabidopsis associated with distinct environmental conditions

Over-Expression of Phosphoserine Aminotransferase-Encoding Gene (AtPSAT1) Prompts Starch Accumulation in L. turionifera under Nitrogen Starvation

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