Trehalose 6-Phosphate Regulates Photosynthesis and Assimilate Partitioning in Reproductive Tissue

Abstract

Transgenic maize (Zea mays) that expresses rice (Oryza sativa) TREHALOSE PHOSPHATE PHOSPHATASE1 (TPP1) from the rice MADS6 promoter, which is active over the flowering period, produces higher yields than wild type. This yield increase occurs with or without drought conditions during flowering. To understand the mechanistic basis of the increased yield, we characterized gene expression and metabolite profiles in leaves and developing female reproductive tissue, comprising florets, node, pith, and shank, over the flowering period with and without drought. The MADS6 promoter was most active in the vasculature, particularly phloem companion cells in florets and pith, consistent with the largest decreases in trehalose 6-phosphate (T6P) levels (2- to 3-fold) being found in pith and florets. Low T6P led to decreased gene expression for primary metabolism and increased gene expression for secondary metabolism, particularly lipid-related pathways. Despite similar changes in gene expression, the pith and floret displayed opposing assimilate profiles: sugars, sugar phosphates, amino acids, and lipids increased in florets, but decreased in pith. Possibly explaining this assimilate distribution, seven SWEET genes were found to be up-regulated in the transgenic plants. SnRK1 activity and the expression of the gene for the SnRK1 beta subunit, expression of SnRK1 marker genes, and endogenous trehalose pathway genes were also altered. Furthermore, leaves of the transgenic maize maintained a higher photosynthetic rate for a longer period compared to wild type. In conclusion, we found that decreasing T6P in reproductive tissues down-regulates primary metabolism and up-regulates secondary metabolism, resulting in different metabolite profiles in component tissues. Our data implicate T6P/ SnRK1 as a major regulator of whole-plant resource allocation for crop yield improvement.

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References 44

1. 1.

   Baena-González E, Hanson J (2017 ) Shaping plant development through the SnRK1-TOR metabolic regulators. Curr Opin Plant Biol 35: 152–157

   Not in our library10.1016/j.pbi.2016.12.004

2. 2.

   Baena-González E, Rolland F, Thevelein JM, Sheen J (2007 ) A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938–942

   Not in our library10.1038/nature06069

3. 3.

   Bezrutczyk M, Hartwig T, Horshman M, Nian Char S, Yang J, Yang B, Frommer WB, Sosso D (2017 ) Impaired phloem loading in genome-edited triple knock-out mutants of SWEET13 sucrose transporters. bioRxiv

   Not in our library10.1111/nph.15021

4. 4.

   Boyer JS, Byrne P, Cassman KG, Cooper M, Delmer D, Greene T, Gruis F, Habben J, Hausmann N, Kenny N, (2013 ) The US drought of 2012 in perspective: A call to action. Global Food Security 2: 139–143

   Not in our library

5. 5.

   Boyer JS, McLaughlin JE (2007 ) Functional reversion to identify controlling genes in multigenic responses: analysis of floral abortion. J Exp Bot 58: 267–277

   Not in our library10.1093/jxb/erl177

6. 6.

   Boyer JS, Westgate ME (2004 ) Grain yields with limited water. J Exp Bot 55: 2385–2394

   Not in our library10.1093/jxb/erh219

7. 7.

   Braun DM, Wang L, Ruan Y-L (2014 ) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. J Exp Bot 65: 1713–1735

   Not in our library10.1093/jxb/ert416

8. 8.

   Brychkova G, Alikulov Z, Fluhr R, Sagi M (2008 ) A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. Plant J 54: 496–509

   Not in our library10.1111/j.1365-313x.2008.03440.x

9. 9.

   Collier R, Tegeder M (2012 ) Soybean ureide transporters play a critical role in nodule development, function and nitrogen export. Plant J 72: 355–367

   Not in our library10.1111/j.1365-313x.2012.05086.x

10. 10.

    Coneva V, Simopoulos C, Casaretto JA, El-Kereamy A, Guevara DR, Cohn J, Zhu T, Guo L, Alexander DC, Bi YM, McNicholas PD, Rothstein SJ (2014 ) Metabolic and co-expression network-based analyses associated with nitrate response in rice. BMC Genomics

    Not in our library10.1186/1471-2164-15-1056

11. 11.

    Cortina C, Culiáñez-Macià FA (2005 ) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169: 75–82

    Not in our library

12. 12.

    Delatte TL, Sedijani P, Kondou Y, Matsui M, de Jong GJ, Somsen GW, Wiese-Klinkenberg A, Primavesi LF, Paul MJ, Schluepmann H (2011 ) Growth arrest by trehalose-6-phosphate: an astonishing case of primary metabolite control over growth by way of the SnRK1 signaling pathway. Plant Physiol 157: 160–174

    Not in our library10.1104/pp.111.180422

13. 13.
    Carbon source–sink relationship in Arabidopsis thaliana: the role of sucrose transporters · 2017

    No notice
14. 14.

    Figueroa CM, Feil R, Ishihara H, Watanabe M, Kölling K, Krause U, Höhne M, Encke B, Plaxton WC, Zeeman SC, (2016 ) Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability. Plant J 85: 410–423

    Not in our library10.1111/tpj.13114

15. 15.

    Henry C, Bledsoe SW, Siekman A, Kollman A, Waters BM, Feil R, Stitt M, Lagrimini LM (2014 ) The trehalose pathway in maize: conservation and gene regulation in response to the diurnal cycle and extended darkness. J Exp Bot 65: 5959–5973

    Not in our library10.1093/jxb/eru335

16. 16.

    Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005 ) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118–11123

    Not in our library10.1073/pnas.0503410102

17. 17.
    Ultrafast and memory-efficient alignment of short DNA sequences to the human genome · 2009

    No notice
18. 18.

    Li L, Stoeckert CJ Jr, Roos DS (2003 ) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189

    Not in our library10.1101/gr.1224503

19. 19.

    Lunn JE, Feil R, Hendriks JH, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajirezaei MR, Stitt M (2006 ) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397: 139–148

    Not in our library10.1042/bj20060083

20. 20.

    Martinez-Barajas E, Delatte T, Schluepmann H, de Jong GJ, Somsen GW, Nunes C, Primavesi LF, Coello P, Mitchell RAC, Paul MJ (2011 ) Wheat grain development is characterised by remarkable T6P accumulation pre-grain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity. Plant Physiology 156: 373–381

    Not in our library10.1104/pp.111.174524

21. 21.

    Martins MCM, Hejazi M, Fettke J, Steup M, Feil R, Krause U, Arrivault S, Vosloh D, Figueroa CM, Ivakov A, (2013 ) Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol 163: 1142–1163

    Not in our library10.1104/pp.113.226787

22. 22.

    Nuccio ML, Wu J, Mowers R, Zhou H-P, Meghji M, Primavesi LF, Paul MJ, Chen X, Gao Y, Haque E, (2015 ) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat Biotechnol 33: 862–869

    Not in our library10.1038/nbt.3277

23. 23.

    Nunes C, O’Hara, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, et al. (2013 a) The T6P/ SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162: 1720–1732

    Not in our library10.1104/pp.113.220657

24. 24.

    Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Sagar R, Fevereiro PS, Davis BG, Paul MJ (2013 b) Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol Biochem 63: 89–98

    Not in our library10.1016/j.plaphy.2012.11.011

25. 25.

    Paul MJ, Foyer CH (2001 ) Sink regulation of photosynthesis. J Exp Bot 52: 1383–1400

    Not in our library10.1093/jexbot/52.360.1383

26. 26.

    Ramon M, De Smet I, Vandesteene L, Naudts M, Leyman B, Van Dijck P, Rolland F, Beeckman T, Thevelein JM (2009 ) Extensive expression regulation and lack of heterologous enzymatic activity of the Class II trehalose metabolism proteins from Arabidopsis thaliana. Plant Cell Environ 32: 1015–1032

    Not in our library10.1111/j.1365-3040.2009.01985.x

27. 27.
    Yield Trends Are Insufficient to Double Global Crop Production by 2050 · 2013

    No notice
28. 28.
    GC-Content Normalization for RNA-Seq Data · 2011

    No notice
29. 29.

    Robinson MD, McCarthy DJ, Smyth GK (2010 ) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140

    Not in our library10.1093/bioinformatics/btp616

30. 30.

    Romero C, Bellés JM, Vayá JL, Serrano R, Culiáñez-Macià FA (1997 ) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201: 293–297

    Not in our library10.1007/s004250050069

31. 31.

    Ruiz-Salas J-L, Ruiz-Medrano R, Montes-Horcasitas MC, Agreda-Laguna KA, Hinojosa-Moya J, Xoconostle-Cazares B (2016 ) Vascular expression of trehalose phosphate synthase1 (TPS1) induces flowering in Arabidopsis. Plant Omics 9: 344–351

    Not in our library

32. 32.

    Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003 ) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6849–6854

    Not in our library10.1073/pnas.1132018100

33. 33.

    Schluepmann H, van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S (2004 ) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol 135: 879–890

    Not in our library10.1104/pp.104.039503

34. 34.

    Schussler JR, Westgate ME (1991 a) Maize kernel set at low water potential: II. Sensitivity to reduced assimilates at pollination. Crop Sci 31: 1196–1203

    Not in our library

35. 35.

    Schussler JR, Westgate ME (1991 b) Maize kernel set at low water potential: I. Sensitivity to reduced assimilates during early kernel growth. Crop Sci 31: 1189–1195

    Not in our library

36. 36.

    Takagi H, Ishiga Y, Watanabe S, Konishi T, Egusa M, Akiyoshi N, Matsuura T, Mori IC, Hirayama T, Kaminaka H, (2016 ) Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner. J Exp Bot 67: 2519–2532

    Not in our library10.1093/jxb/erw071

37. 37.

    Trapnell C, Pachter L, Salzberg SL (2009 ) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111

    Not in our library10.1093/bioinformatics/btp120

38. 38.
    Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture · 2014

    No notice
39. 39.

    Wingler A, Delatte TL, O'Hara LE, Primavesi LF, Jhurreea D, Paul MJ, Schluepmann H (2012 ) Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158: 1241–1251

    Not in our library10.1104/pp.111.191908

40. 40.

    Wu D, Lim E, Vaillant F, Asselin-Labat ML, Visvader JE, Smyth GK (2010 ) ROAST: rotation gene set tests for complex microarray experiments. Bioinformatics 26: 2176–2182

    Not in our library10.1093/bioinformatics/btq401

41. 41.
    The sucrose–trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P · 2014

    No notice
42. 42.

    Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009 ) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149: 1860–1871

    Not in our library10.1104/pp.108.133934

43. 43.

    Zinselmeier C, Lauer MJ, Boyer JS (1995 a) Reversing drought-induced losses in grain yield: sucrose maintains embryo growth in maize. Crop Sci 35: 1390–1400

    Not in our library

44. 44.

    Zinselmeier C, Westgate ME, Schussler JR, Jones RJ (1995 b) Low water potential disrupts carbohydrate metabolism in maize (Zea mays L.) ovaries. Plant Physiol 107: 385–391

    Not in our library10.1104/pp.107.2.385

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