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Chemical intervention in plant sugar signalling increases yield and resilience

Nature volume 540, pages 574–578 (2016)Cite this article

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Abstract

The pressing global issue of food insecurity due to population growth, diminishing land and variable climate can only be addressed in agriculture by improving both maximum crop yield potential and resilience1,2. Genetic modification is one potential solution, but has yet to achieve worldwide acceptance, particularly for crops such as wheat3. Trehalose-6-phosphate (T6P), a central sugar signal in plants, regulates sucrose use and allocation, underpinning crop growth and development4,5. Here we show that application of a chemical intervention strategy directly modulates T6P levels in planta. Plant-permeable analogues of T6P were designed and constructed based on a ‘signalling-precursor’ concept for permeability, ready uptake and sunlight-triggered release of T6P in planta. We show that chemical intervention in a potent sugar signal increases grain yield, whereas application to vegetative tissue improves recovery and resurrection from drought. This technology offers a means to combine increases in yield with crop stress resilience. Given the generality of the T6P pathway in plants and other small-molecule signals in biology, these studies suggest that suitable synthetic exogenous small-molecule signal precursors can be used to directly enhance plant performance and perhaps other organism function.

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Figure 1: Design and synthesis of signalling precursors of T6P.
Figure 2: In planta uptake of signalling precursors and T6P release.
Figure 3: Mass spectometry imaging of treated leaves.
Figure 4: In planta T6P release and sugar metabolism over time.
Figure 5: Increased crop yield.
Figure 6: Increased crop resilience.

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Acknowledgements

We thank the BBSRC Selective Chemical Intervention in Biological Systems initiative (grant reference BB/D006112/1), the BBSRC Sparking Impact initiative and ICL Innovations for funding. We thank R. H. Bromilow, S. Powers, E. Tobolkina, for advice and J. Wickens for technical assistance. NiCE-MSI is supported by the 3D NanoSIMS and AIMS-HIGHER projects of the Chemical and Biological programme of the National Measurement System of the UK Department of Business, Innovation and Skills. B.G.D. was a Royal Society Wolfson Research Merit Award recipient during the period of research. Rothamsted Research receives strategic funding from the BBSRC.

Author information

Author notes

  1. Ram Sagar

    Present address: †Present address: Department of Chemistry, School of Natural Sciences, Shiv Nadar University, Greater Noida 201 314, India.,

  2. Cara A. Griffiths, Ram Sagar and Yiqun Geng: These authors contributed equally to this work.

Authors and Affiliations

  1. Plant Biology and Crop Science, Rothamsted Research, AL5 2JQ, Harpenden, Hertfordshire, UK

    Cara A. Griffiths, Lucia F. Primavesi & Matthew J. Paul

  2. Department of Chemistry, Chemistry Research Laboratory, University of Oxford, OX1 3TA, Mansfield Road, Oxford, UK

    Ram Sagar, Yiqun Geng, Mitul K. Patel & Benjamin G. Davis

  3. National Centre of Excellence in Mass Spectrometry Imaging (NiCE-MSI), National Physical Laboratory (NPL), TW11 0LW, Teddington, Middlesex, UK

    Melissa K. Passarelli, Ian S. Gilmore, Rory T. Steven & Josephine Bunch

  4. School of Pharmacy, University of Nottingham, NG7 2RD, Nottingham, UK

    Josephine Bunch

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Contributions

C.A.G., R.S. and Y.G. are joint first authors. C.A.G., R.S., Y.G. and L.F.P. performed experiments. R.S., Y.G. and M.K.Pat. synthesized compounds. Y.G. and M.K.Pas., I.S.G., R.T.S., J.B. and B.G.D. performed and/or analysed the mass spectrometry imaging. Y.G. and B.G.D. performed and/or analysed the tandem mass spectrometry. C.A.G., R.S., Y.G., L.F.P., M.J.P. and B.G.D. designed and analysed the experiments. M.J.P. and B.G.D. wrote the paper. All authors read and commented on the paper.

Corresponding authors

Correspondence to Matthew J. Paul or Benjamin G. Davis.

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Extended data figures and tables

Extended Data Figure 1 The central role of T6P in plants and design of a chemical strategy for the control of T6P production.

a, Photosynthesis generates sucrose, which is translocated to growing regions of the plant. Inside the cell, a pool of core metabolites are substrates for biosynthetic processes that determine growth and productivity. T6P is synthesized from UDPG and G6P by trehalose 6-phosphate synthase (TPS) and therefore reflects the abundance of sucrose. It is broken down by trehalose phosphate phosphatase (TPP). Increasing T6P stimulates starch synthesis and inhibits SnRK1, a protein kinase central to energy conservation and survival during energy deprivation. Inhibition of SnRK1 by T6P thus diverts carbon skeleton consumption into biosynthetic processes. b, The trehalose biosynthetic pathway. c, T6P is plant-impermeable. Plant-permeable variants allowed subsequent photo-activated release. d, Generalized mechanism of light-activated release of precursors. e, Release of T6P by light irradiation from signalling precursors 1–4 in vitro. 31P nuclear magnetic resonance spectroscopy at different time points of light irradiation confirming the activation of signalling precursors (1–4) and release of T6P. Time points for compound 1: 0, 30, 60, 150 and 360 min; for compound 2: 0, 60, 120, 300, 420 and 600 min; for compound 3: 0, 15, 30, 45 and 60 min; and for compound 4: 0, 60, 120, 240, 360 and 420 min. f, g, 1H (f) and 31P (g) nuclear magnetic resonance spectra, after complete photolysis of the signalling precursor confirming the release of T6P.

Extended Data Figure 2 Inhibition of SnRK1.

Signalling precursors (1–4), T6P released from 1–4 (r1, r2, r3, r4) and T6P standard (T6P) were tested for inhibition of SnRK1 activity. T6P (0.26 mM) inhibits SnRK1 activity to approximately 36% of the original activity. Signalling-precursor compounds show no such inhibition, whereas UV-released compounds show the same inhibition as free T6P. SnRK1 activity was determined by the level of incorporation of phosphate into a peptide substrate (min−1 mg−1 protein). (Data are shown as mean ± s.e.m.; n = 3). The activities of assays treated with precursors or released T6P were not significantly different from their controls (P < 0.001, LSD) using one-way ANOVA of data transformed with a natural log scale.

Extended Data Figure 3 In planta uptake analysis of signalling precursors 1–4.

a, Schematic of protocol used for uptake analysis. b, Calibration curves for oNB-T6P (1), DMNB-T6P (2), oNPE-T6P (3) and mono-DMNB-T6P (4), respectively. Data are shown as mean ± s.e.m.; (n = 2). c, HPLC (left) and mass spectrometry (right) data, [M + Na]+ or [M − H]−, of pure signalling precursors 1–4. d, HPLC (left) and mass spectometry (right) data, [M + Na]+ or [M − H]−, of plant samples after treatment with signalling precursors 1–4. In 3, the partially uncaged molecule also accumulated and was detected (coloured light blue).

Extended Data Figure 4 Extraction and quantification of T6P.

a, Schematic of the protocol used for preparation of samples for T6P quantification. LLE, liquid/liquid extraction; SPE, solid phase extraction; AEC–MS, anion exchange chromatography–mass spectrometry. b, Liquid chromatograms of T6P, S6P and 2DG6P separation (top) using conditions optimized in Supplementary Table 8 (entry 7) and the representative LC–MS chromatograms of extraction samples treated with signalling precursors (middle) and water control (bottom). c, d, Liquid chromatograms of different concentrations of T6P (500, 250, 100, 50, 25, 10 or 5 μM) using a constant concentration (100 μM) of 2DG6P as an internal standard. e, Resulting calibration curves of the T6P peak area and T6P/2DG6P ratio against T6P concentrations (in μM) in water as well as in the plant matrix. f–h, LC–MS/MS analysis of T6P and S6P from samples of plant treated with compound 2. f, Fragmentation patterns of T6P (top) and S6P (bottom) by quadrupole time-of-fight tandem mass spectrometry (QToF–MS/MS) in negative ion mode. g, Fragmentation patterns of T6P (top) and S6P (middle) by triple quadrupole tandem mass spectrometry (QqQ–MS/MS) in negative ion mode and the T6P fragment ions tracking in the plant matrix (bottom). h, HPLC chromatograms of T6P/S6P by selected ion recording (SIR) of the intact molecular ion (m/z 421.0) and multiple reaction monitoring (MRM) of the fragment ions give the same retention time for each compound. i, The LC–MS quantification method through SIR and LC–MS/MS quantification method through MRM of the T6P level in the DMNB-T6P 2-treated plant sample. From bottom to top: integration of the T6P trace (2,661) using SIR of m/z 421.0, integration of the T6P trace (2,550) using MRM of m/z 78.6, 96.3, 138.7, 241.0 and 421.0, integration for each fragment ion m/z 78.6 (801), m/z 96.3 (868), m/z 138.7 (76), m/z 241.0 (404) and m/z 421.0 (392).

Extended Data Figure 5 Analysis of A. thaliana plantlets following treatment.

a–c, Phenotype analysis. a, Fresh weight of plantlets versus concentration of signalling precursors of T6P (1–4) and G6P precursors (14–17) in medium after three days (72 h) of uptake. Data are shown as mean ± s.e.m.; n = 3. Each T6P precursor is shown (top) together with its G6P analogue (bottom). Visual appearance of a typical plantlet was analysed for a given concentration of precursors at the point of harvest. b, Phenotype of plants at the end of light treatments. Plants were allowed to take up compounds for 72 h and were then treated the next day with light treatments. Light treatments: GL, growth light irradiance 250 μmol m−2 s−1. UV 8 W and UV 100 W were growth light irradiance supplemented with UV light (365 nm). Daylight, part sun/part cloud; irradiance between 250 μmol m−2 s−1 under cloud and 1,440 μmol m−2 s−1 under full sun. Compounds were fed to the plants to a final concentration of 1 mM. Phenotype of plants fed with compound 3 at a reduced final concentration of 0.1 mM are shown in the right-hand panel. Scale, diameter of the plastic tube mouth = 10 mm. c, Typical A. thaliana phenotypes in the starch experiment. Plants were treated with a final medium concentration of 0.1 mM compound or water for 72 h and then exposed to 8-h, 8 W UV treatment. The plants were allowed to recover for another 24 h and were harvested at the end of the day and the starch content was measured. No significant phenotypic differences were observed between treatments. Water (left), 0.1 mM oNPE-T6P (compound 3) (middle), oNPE-G6P(1-OMe) (compound 16) (right). Scale, tube diameter = 10 mm. d–g, Biosynthetic effects of increasing T6P in planta. d, Starch level at the end of the day in UV-treated (8 W, 23 μmol m−2 s−1, 8 h) plants fed with compound 3 + UV is significantly higher than plants treated with water + UV (n = 9, data are shown as mean ± s.e.m.). Samples for starch were taken 1 day after UV treatment. e, ADP-glucose pyrophosphorylase (AGPase) activity is increased in UV + compound 3 plants compared to compound 3 only, UV only, water only, UV + water-treated plants and plants treated with compound 16 (n = 3, data are shown as mean ± s.e.m.). f, Starch synthesis rate in UV-treated (20 μmol m−2 s−1, 8 h) plants treated with compound 3 (data are shown as mean ± s.e.m., n = 3). g, Starch level at the beginning (data are shown as mean ± s.e.m.; n = 3) and at the end (data are shown as mean ± s.e.m.; n = 4) of the day in UV (20 μmol m−2 s−1, 8 h) + water-treated (solid circles) and UV + compound 3-treated (empty circles) plants. A. thaliana used in e–g were grown at a light regime of 12 h day–12 h night, at 250 μmol m−2 s−1, and 23 °C day/18 °C night temperatures, treated with compounds 18 d after sowing, and exposed to UV light 72 h after addition of the compound. Asterisks in d–f denote significance according to ANOVA (P = 0.002). Asterisk in g denotes significance by one-way ANOVA (LSD 5% = 11.19).

Extended Data Figure 6 Quantification of in planta metabolites.

a, LC–MS chromatograms of trehalose, sucrose, glucose and fructose separation using a HILIC column, for details see Supplementary Information. b, Liquid chromatograms and peak areas of different concentrations of trehalose (100, 50, 25, 10 or 5 μM) and glucose (500, 250, 100, 50, 25, 10 or 5 μM). c, Calibration curves of the trehalose peak area against the concentrations (in μM) and glucose peak area against the concentrations (in μM). d, e, Same as Fig. 4, 7-day-old A. thaliana seedlings grown in liquid culture were treated with 1 mM of compounds 3 or 2, control seedlings were treated with water. Seedlings were left under growth lights to allow for uptake of the signalling precursors for 24 h, before exposure to 23 μmol m−2 s−1 UV for 2 h. Measurements were taken 1 day after uptake (pre-UV), 30, 60 and 120 min after initiation of UV treatment, and 1 and 2 d after initiation of UV treatment. See Fig. 4 for T6P content, trehalose content, sucrose content, glucose content; here fructose content (d)and Fresh weight biomass (e) are shown. *P < 0.05); **P < 0.01 (Student’s t-test). Data are shown as mean ± s.e.m. (n = 3).

Extended Data Figure 7 Dynamics of 13C-T6P, 13C-trehalose, 13C-glucose and T6P in A. Thaliana treated with 13C-labelled precursor 2*.

1 mM of DMNB-13C-T6P (2*) was added to the growth medium of 7-day-old A. thaliana seedlings. The plants were left under growth light to allow uptake for 24 h and the uncaging was performed under 23 μmol m−2 s−1 UV for 2 h. Samples were harvested for analysis at different time points: pre-UV, 30, 60 and 120 min (after onset of UV irradiation) and 1 and 2 days after UV irradiation. a, Synthesis of universally 13C-labelled 2* in essentially the same manner as for 2. b, Amount of 13C-T6P released over time in planta. c, Amount of 13C-trehalose accumulated. d, Amount of 13C-glucose accumulated. e, Amount of endogenous T6P. f, Overview of 13C tracking of T6P and metabolites. Data are shown as mean ± s.e.m.; n = 3; *P < 0.05; **P < 0.01 (Student’s t-test).

Extended Data Figure 8 Synthesis, in vitro SnRK1 inhibition studies and in planta uptake analysis of G6P(1-OMe) precursors 14–17.

a, Design and synthesis of oNB-G6P(1-OMe) (14), DMNB-G6P(1-OMe) (15), oNPE-G6P(1-OMe) (16) and mono-DMNB-G6P(1-OMe) (17). b, Lack of inhibition of SnRK1 by G6P(1-OMe) analogues. Data are shown as mean ± s.e.m., (n = 3). c, HPLC and mass spectometry data, [M + Na]+ or [M − H]−, of pure G6P(1-Ome) precursors 14–17. For HPLC conditions see the Supplementary Information section 1. d, HPLC and mass spectometry data, [M + Na]+ or [M − H]−, of uptaken G6P(1-Ome) precursors14–17 in planta. e, Calibration curves for compounds 15, 16 and 17, respectively (n = 2 in all cases).

Extended Data Figure 9 Transcript abundance of genes involved in starch synthesis and SnRK1 marker genes in response to caged T6P precursor application of 7-day-old A. thaliana seedlings in liquid culture.

Seedlings were treated with a final concentration of 1 mM of compounds 2 or 3, uptake was allowed for 1 d under the growth lights, before treatment with 23 μmol m−2 s−1 UV light for 2 h to facilitate uncaging. a, b, Transcript fold change after 60 min of UV treatment (a) and 1 d after UV treatment (b) of SnRK1 marker genes. Marker genes normally downregulated by SnRK1: TPS5, UDPGDH (At3g29360) and bZIP11, and marker genes normally upregulated by SnRK1: TPS8, ΒGAL and ASN1. c, Transcript fold change of starch synthesis genes after 60 min of UV treatment. Genes involved in starch synthesis: APL3, SS3, BE1 and GBSS1. d, Transcript fold change after 60 min of UV treatment for starch degradation genes. Genes involved in starch degradation: BAM1, BAM3, BAM4 and GWD3. Changes in transcripts for enzymes of degradation were more equivocal with GWD3 increasing and BAM genes showing small changes or decreasing (BAM3). All data were normalized to a ubiquitin control. Data are shown as mean ± s.e.m. of three independent samples.

Extended Data Figure 10 Additional effects in wheat.

a, Chlorophyll content of leaves after anthesis of ear treatments. b, Chlorophyll content of leaves after anthesis of whole-plant treatments. c–e, T6P release and metabolism in wheat. Developing wheat grain were treated with T6P, or compounds 2 or 3 (all 1 mM) 5 or 10 days after anthesis (DPA) and harvested 1 day later. c, Amount of T6P in wheat grains (n = 3; data are shown as mean ± s.e.m.). d, Trehalose (n = 3; data are shown as mean ± s.e.m.). e, Sucrose (n = 3; data are shown as mean ± s.e.m.). *P < 0.05; **P < 0.01 (Student’s t-test). f, Dose response grain yield per plant to T6P precursors (0.1, 1 or 10 mM oNPE-T6P (3) or DMNB-T6P (2) and water, T6P and trehalose controls) sprayed to ears (5 ml) or to the whole plant (50 ml) at 5, 10, 15 and 20 days after anthesis. g, Grain yield per ear in response to a single time point spray (5 ml to the ear at 10 days after anthesis). *P < 0.05 (f, g) compared to water control (Student’s t-test). Data are shown as mean ± s.e.m. (n = 6).

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Griffiths, C., Sagar, R., Geng, Y. et al. Chemical intervention in plant sugar signalling increases yield and resilience. Nature 540, 574–578 (2016). https://doi.org/10.1038/nature20591

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