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From Arabidopsis to Crops: The Arabidopsis QQS Orphan Gene Modulates Nitrogen Allocation Across Species

  • Seth O’Conner
  • Andrea Neudorf
  • Wenguang Zheng
  • Mingsheng Qi
  • Xuefeng Zhao
  • Chuanlong Du
  • Dan Nettleton
  • Ling Li
Chapter

Abstract

To enhance the nitrogen use efficiency (NUE) of crops to increase yields, one approach is to develop crops with improved NUE. Qua quine starch (QQS), a species-specific orphan gene present only in Arabidopsis thaliana, has a novel, unexpected functionality in regulation of carbon and nitrogen allocation. Approximately 0.5–8% of genes in a given species are uniquely present in that species, having no homologs in other species. They represent a significant fraction of eukaryotic and prokaryotic genomes, and are thought to be a determinant of the character of a species. However, little is known about their functional significance. QQS can affect the important trait of protein content when expressed in other species, including soybean, maize, and rice. Understanding QQS functions has multiple impacts, revealing how plants allocate precious carbon and nitrogen resources. Here, we report that QQS interactor nuclear factor Y subunit C4 (NF-YC4) affects carbon and nitrogen allocation to protein in soybean and maize. RNA-sequencing analyses of the QQS mutant materials have identified candidate genes involved in regulation of nitrogen allocation. QQS and its related network may be used as a tool to increase the protein content in crops and to study the nitrogen allocation network.

Keywords

QQS Orphan Nitrogen allocation Arabidopsis thaliana Glycine max Zea mays 

Notes

Acknowledgements

We thank Diane Luth, Bronwyn Frame, and Kan Wang at ISU PTF for soybean and maize transformation; Kent Berns for field management; Charles Hurburgh and Glen Rippke at ISU Grain Quality Laboratory for NIRS analysis of soybean and maize seed composition; and Eurofins for Kjeldahl analysis. The transcriptome sequencing was conducted in conjunction with BGI. We thank BGI for contributing its expertise in genomic sequencing and bioinformatics analysis to provide processed sequencing data. This material is based in part upon work supported by: National Science Foundation (L.L. as Co-PI on MCB-0951170), United Soybean Board (2287 to L.L.), Iowa Soybean Association (to L.L.), Amfora Inc (to L.L.), ISU Research Foundation (to L.L.), and Center for Metabolic Biology at ISU.

References

  1. Arendsee ZW, Li L, Wurtele ES (2014) Coming of age: orphan genes in plants. Trends Plant Sci 19:698–708PubMedCrossRefGoogle Scholar
  2. Ascencio-Ibáñez JT, Sozzani R, Lee T-J, Chu T-M, Wolfinger RD, Cella R, Hanley-Bowdoin L (2008) Global analysis of arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148:436–454PubMedPubMedCentralCrossRefGoogle Scholar
  3. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448(7156):938–942PubMedCrossRefGoogle Scholar
  4. Beatty PH, Klein MS, Fischer JJ, Lewis IA, Muench DG, Good AG (2016) Understanding plant nitrogen metabolism through metabolomics and computational approaches. Plants (Basel) 5:39CrossRefGoogle Scholar
  5. Beatty PH, Shrawat AK, Carroll RT, Zhu T, Good AG (2009) Transcriptome analysis of nitrogen-efficient rice over-expressing alanine aminotransferase. Plant Biotechnol J 7:562–576PubMedCrossRefGoogle Scholar
  6. Bullard JH, Purdom E, Hansen KD, Dudoit S (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11:94PubMedPubMedCentralCrossRefGoogle Scholar
  7. Che P, Weaver LM, Wurtele ES, Nikolau BJ (2003) The role of biotin in regulating 3-methylcrotonyl-coenzyme a carboxylase expression in Arabidopsis. Plant Physiol 131:1479–1486PubMedPubMedCentralCrossRefGoogle Scholar
  8. Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37:853–863PubMedCrossRefGoogle Scholar
  9. Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J 26:89–100PubMedCrossRefGoogle Scholar
  10. Delatte T, Trevisan M, Parker ML, Zeeman SC (2005) Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant J 41:815–830PubMedCrossRefGoogle Scholar
  11. Delatte T, Umhang M, Trevisan M, Eicke S, Thorneycroft D, Smith SM, Zeeman SC (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. J Biol Chem 281:12050–12059PubMedCrossRefGoogle Scholar
  12. Ding ZJ, Yan JY, Xu XY, Yu DQ, Li GX, Zhang SQ, Zheng SJ (2014) Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79:13–27PubMedCrossRefGoogle Scholar
  13. Doyle EA, Lane AM, Sides JM, Mudgett MB, Monroe JD (2007) An alpha-amylase (At4g25000) in Arabidopsis leaves is secreted and induced by biotic and abiotic stress. Plant Cell Environ 30:388–398PubMedCrossRefGoogle Scholar
  14. Eastmond PJ (2006) SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18:665–675PubMedPubMedCentralCrossRefGoogle Scholar
  15. Eastmond PJ, Dennis DT, Rawsthorne S (1997) Evidence that a malate/inorganic phosphate exchange translocator imports carbon across the leucoplast envelope for fatty acid synthesis in developing castor seed endosperm. Plant Physiol 114:851–856PubMedPubMedCentralCrossRefGoogle Scholar
  16. Edner C, Li J, Albrecht T, Mahlow S, Hejazi M, Hussain H, Kaplan F, Guy C, Smith SM, Steup M, Ritte G (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial beta-amylases. Plant Physiol 145:17–28PubMedPubMedCentralCrossRefGoogle Scholar
  17. Fernandez AP, Strand A (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513PubMedCrossRefGoogle Scholar
  18. Fukushima A, Kusano M, Mejia RF, Iwasa M, Kobayashi M, Hayashi N, Watanabe-Takahashi A, Narisawa T, Tohge T, Hur M, Wurtele ES, Nikolau BJ, Saito K (2014) Metabolomic characterization of knockout mutants in Arabidopsis: development of a metabolite profiling database for knockout mutants in Arabidopsis. Plant Physiol 165:948–961PubMedPubMedCentralCrossRefGoogle Scholar
  19. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, Dorken G, Halliday K, Smith AM, Smith SM, Zeeman SC (2008) {beta}-Amylase4, a noncatalytic protein required for starch breakdown, acts upstream of three active {beta}-Amylases in Arabidopsis chloroplasts. Plant Cell 20:1040–1058PubMedPubMedCentralCrossRefGoogle Scholar
  20. Gollery M, Harper J, Cushman J, Mittler T, Girke T, Zhu JK, Bailey-Serres J, Mittler R (2006) What makes species unique? The contribution of proteins with obscure features. Genome Biol 7:R57PubMedPubMedCentralCrossRefGoogle Scholar
  21. Gollery M, Harper J, Cushman J, Mittler T, Mittler R (2007) POFs: what we don’t know can hurt us. Trends Plant Sci 12:492–496PubMedCrossRefGoogle Scholar
  22. Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9:597–605PubMedCrossRefGoogle Scholar
  23. Han M, Okamoto M, Beatty PH, Rothstein SJ, Good AG (2015) The genetics of nitrogen use efficiency in crop plants. Annu Rev Genet 49:269–289PubMedCrossRefGoogle Scholar
  24. Hedges SB, Kumar S (2009) The timetree of life. Oxford University Press, New York, USAGoogle Scholar
  25. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387PubMedCrossRefGoogle Scholar
  26. Ishihara H, Obata T, Sulpice R, Fernie AR, Stitt M (2015) Quantifying protein synthesis and degradation in arabidopsis by dynamic 13CO2 labeling and analysis of enrichment in individual amino acids in their free pools and in protein. Plant Physiol 168:74–93PubMedPubMedCentralCrossRefGoogle Scholar
  27. Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679PubMedPubMedCentralCrossRefGoogle Scholar
  28. Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryot Cell 12:776–793PubMedPubMedCentralCrossRefGoogle Scholar
  29. Jones DC, Zheng W, Huang S, Du C, Zhao X, Yennamalli RM, Sen TZ, Nettleton D, Wurtele ES, Li L (2016) A clade-specific Arabidopsis gene connects primary metabolism and senescence. Front Plant Sci 7:983PubMedPubMedCentralGoogle Scholar
  30. Kahle J, Baake M, Doenecke D, Albig W (2005) Subunits of the heterotrimeric transcription factor NF-Y are imported into the nucleus by distinct pathways involving importin beta and importin 13. Mol Cell Biol 25:5339–5354PubMedPubMedCentralCrossRefGoogle Scholar
  31. Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A, Flugge UI (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 10:105–117PubMedPubMedCentralCrossRefGoogle Scholar
  32. Kaplan F, Guy CL (2004) beta-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135:1674–1684PubMedPubMedCentralCrossRefGoogle Scholar
  33. Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch TC (2009) More than just orphans: are taxonomically-restricted genes important in evolution? Trends Genet 25:404–413PubMedCrossRefGoogle Scholar
  34. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540PubMedCrossRefGoogle Scholar
  35. Kumimoto RW, Zhang Y, Siefers N, Holt BF 3rd (2010) NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J 63:379–391PubMedCrossRefGoogle Scholar
  36. Laby RJ, Kim D, Gibson SI (2001) The ram1 mutant of Arabidopsis exhibits severely decreased beta-amylase activity. Plant Physiol 127:1798–1807PubMedPubMedCentralCrossRefGoogle Scholar
  37. Laloum T, De Mita S, Gamas P, Baudin M, Niebel A (2013) CCAAT-box binding transcription factors in plants: y so many? Trends Plant Sci 18:157–166PubMedCrossRefGoogle Scholar
  38. Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA (1999) An Arabidopsis gene encoding a chloroplast-targeted beta-amylase. Plant J 20:519–527PubMedCrossRefGoogle Scholar
  39. Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807PubMedCrossRefGoogle Scholar
  40. Lau W, Fischbach MA, Osbourn A, Sattely ES (2014) Key applications of plant metabolic engineering. PLoS Biol 12:e1001879PubMedPubMedCentralCrossRefGoogle Scholar
  41. Levesque-Lemay M, Albani D, Aldcorn D, Hammerlindl J, Keller W, Robert LS (2003) Expression of CCAAT-binding factor antisense transcripts in reproductive tissues affects plant fertility. Plant Cell Rep 21:804–808PubMedGoogle Scholar
  42. Li L, Foster CM, Gan Q, Nettleton D, James MG, Myers AM, Wurtele ES (2009) Identification of the novel protein QQS as a component of the starch metabolic network in Arabidopsis leaves. Plant J 58:485–498PubMedCrossRefGoogle Scholar
  43. Li L, Ilarslan H, James MG, Myers AM, Wurtele ES (2007) Genome wide co-expression among the starch debranching enzyme genes AtISA1, AtISA2, and AtISA3 in Arabidopsis thaliana. J Exp Bot 58:3323–3342PubMedCrossRefGoogle Scholar
  44. Li L, Wurtele ES (2012) Materials and methods for modifying a biochemical component in a plant, U.S. Application 20120222167 A1, U.S. Patent 9157091, U.S. patent and trademark officeGoogle Scholar
  45. Li L, Wurtele ES (2015) The QQS orphan gene of Arabidopsis modulates carbon and nitrogen allocation in soybean. Plant Biotechnol J 13:177–187PubMedCrossRefGoogle Scholar
  46. Li L, Zheng W, Zhu Y, Ye H, Tang B, Arendsee ZW, Jones D, Li R, Ortiz D, Zhao X, Du C, Nettleton D, Scott MP, Salas-Fernandez MG, Yin Y, Wurtele ES (2015) QQS orphan gene regulates carbon and nitrogen partitioning across species via NF-YC interactions. Proc Natl Acad Sci USA 112:14734–14739PubMedCrossRefGoogle Scholar
  47. Liang M, Yin X, Lin Z, Zheng Q, Liu G, Zhao G (2014) Identification and characterization of NF-Y transcription factor families in Canola (Brassica napus L.). Planta 239:107–126PubMedCrossRefGoogle Scholar
  48. Lightfoot DA (2013) Nitrogen fixation and assimilation. In: Kole C (ed) Genomics and breeding for climate-resilient crops, vol 2. Target traits. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 395–413CrossRefGoogle Scholar
  49. Liscombe DK, Facchini PJ (2008) Evolutionary and cellular webs in benzylisoquinoline alkaloid biosynthesis. Curr Opin Biotechnol 19:173–180PubMedCrossRefGoogle Scholar
  50. Litholdo CG Jr, Parker BL, Eamens AL, Larsen MR, Cordwell SJ, Waterhouse PM (2016) Proteomic identification of putative Microrna394 target genes in Arabidopsis thaliana identifies major latex protein family members critical for normal development. Mol Cell Proteomics 15:2033–2047PubMedPubMedCentralCrossRefGoogle Scholar
  51. Liu JZ, Braun E, Qiu WL, Shi YF, Marcelino-Guimaraes FC, Navarre D, Hill JH, Whitham SA (2014) Positive and negative roles for soybean MPK6 in regulating defense responses. Mol Plant Microbe Interact 27:824–834PubMedCrossRefGoogle Scholar
  52. Lloyd JR, Kossmann J, Ritte G (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci 10:130–137PubMedCrossRefGoogle Scholar
  53. Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 138:2280–2291PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218:466–473PubMedCrossRefGoogle Scholar
  55. Lu Y, Steichen JM, Yao J, Sharkey TD (2006) The role of cytosolic alpha-glucan phosphorylase in maltose metabolism and the comparison of amylomaltase in Arabidopsis and Escherichia coli. Plant Physiol 142:878–889PubMedPubMedCentralCrossRefGoogle Scholar
  56. Luhua S, Ciftci-Yilmaz S, Harper J, Cushman J, Mittler R (2008) Enhanced tolerance to oxidative stress in transgenic Arabidopsis plants expressing proteins of unknown function. Plant Physiol 148:280–292PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lund SP, Nettleton D, McCarthy DJ, Smyth GK (2012) Detecting differential expression in RNA-sequence data using quasi-likelihood with shrunken dispersion estimates. Stat Appl Genet Mol Biol 11:1544–6115CrossRefGoogle Scholar
  58. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105:1141–1157PubMedPubMedCentralCrossRefGoogle Scholar
  59. McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10:1011–1025PubMedCrossRefGoogle Scholar
  60. Melis A (2013) Carbon partitioning in photosynthesis. Curr Opin Chem Biol 17:453–456PubMedCrossRefGoogle Scholar
  61. Mentzen WI, Wurtele ES (2008) Regulon organization of Arabidopsis. BMC Plant Biol 8:99PubMedPubMedCentralCrossRefGoogle Scholar
  62. Nardini M, Gnesutta N, Donati G, Gatta R, Forni C, Fossati A, Vonrhein C, Moras D, Romier C, Bolognesi M, Mantovani R (2013) Sequence-specific transcription factor NF-Y displays histone-like DNA binding and H2B-like ubiquitination. Cell 152:132–143PubMedCrossRefGoogle Scholar
  63. Nettleton D, Hwang JTG, Caldo R, Wise R (2006) Estimating the number of true null hypotheses from a histogram of p values. JABES 11:337–356CrossRefGoogle Scholar
  64. Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, Rosso MG, Ache P, Flugge UI, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17:760–775PubMedPubMedCentralCrossRefGoogle Scholar
  65. Niittyla T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303:87–89PubMedCrossRefGoogle Scholar
  66. Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Holt BF 3rd, Mantovani R (2012) The promiscuous life of plant nuclear factor Y transcription factors. Plant Cell 24:4777–4792PubMedPubMedCentralCrossRefGoogle Scholar
  67. Qi M, Zheng W, Zhao X, Hohenstein J, Kandel Y, O'Conner S, Wang Y, Du C, Nettleton D, Macintosh G, Tylka G, Wurtele E, Whitham S, Li L (2018) QQS orphan gene and its interactor NFYC4 reduce susceptibility to pathogens and pests. Plant Biotechnol J https://doi.org/10.1111/pbi.12961
  68. Reiter WD (2008) Biochemical genetics of nucleotide sugar interconversion reactions. Curr Opin Plant Biol 11:236–243PubMedCrossRefGoogle Scholar
  69. Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54:608–620PubMedCrossRefGoogle Scholar
  70. Scheidig A, Frohlich A, Schulze S, Lloyd JR, Kossmann J (2002) Downregulation of a chloroplast-targeted beta-amylase leads to a starch-excess phenotype in leaves. Plant J 30:581–591PubMedCrossRefGoogle Scholar
  71. Schiltz S, Gallardo K, Huart M, Negroni L, Sommerer N, Burstin J (2004) Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol 135:2241–2260PubMedPubMedCentralCrossRefGoogle Scholar
  72. Schneider A, Hausler RE, Kolukisaoglu U, Kunze R, van der Graaff E, Schwacke R, Catoni E, Desimone M, Flugge UI (2002) An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 32:685–699PubMedCrossRefGoogle Scholar
  73. Seo PJ, Kim MJ, Ryu JY, Jeong EY, Park CM (2011) Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism. Nat Commun 2:303PubMedCrossRefGoogle Scholar
  74. Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732PubMedCrossRefGoogle Scholar
  75. Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LE, Loudet O, Colot V, Vincentz M (2013) Extensive natural epigenetic variation at a de novo originated gene. PLoS Genet 9:e1003437PubMedPubMedCentralCrossRefGoogle Scholar
  76. Smith AM, Zeeman SC, Thorneycroft D, Smith SM (2003) Starch mobilization in leaves. J Exp Bot 54:577–583PubMedCrossRefGoogle Scholar
  77. Sparla F, Costa A, Lo Schiavo F, Pupillo P, Trost P (2006) Redox regulation of a novel plastid-targeted beta-amylase of Arabidopsis. Plant Physiol 141:840–850PubMedPubMedCentralCrossRefGoogle Scholar
  78. Steichen JM, Petty RV, Sharkey TD (2008) Domain characterization of a 4-alpha-glucanotransferase essential for maltose metabolism in photosynthetic leaves. J Biol Chem 283:20797–20804PubMedPubMedCentralCrossRefGoogle Scholar
  79. Stitt M (2013) Systems-integration of plant metabolism: means, motive and opportunity. Curr Opin Plant Biol 16:381–388PubMedCrossRefGoogle Scholar
  80. Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism—more than the icing on the cake. Plant J 61:1067–1091PubMedCrossRefGoogle Scholar
  81. Storey JD (2002) A direct approach to false discovery rates. J Royal Stat Soc Ser B (Statistical Methodology) 64:479–498CrossRefGoogle Scholar
  82. Streb S, Delatte T, Umhang M, Eicke S, Schorderet M, Reinhardt D, Zeeman SC (2008) Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell 20:3448–3466PubMedPubMedCentralCrossRefGoogle Scholar
  83. Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, Stitt M (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7:137–155PubMedCrossRefGoogle Scholar
  84. Sweetlove LJ, Fell D, Fernie AR (2008) Getting to grips with the plant metabolic network. Biochem J 409:27–41PubMedCrossRefGoogle Scholar
  85. Thum KE, Shin MJ, Gutierrez RA, Mukherjee I, Katari MS, Nero D, Shasha D, Coruzzi GM (2008) An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis. BMC Syst Biol 2:31PubMedPubMedCentralCrossRefGoogle Scholar
  86. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111PubMedPubMedCentralCrossRefGoogle Scholar
  87. Usadel B, Blasing OE, Gibon Y, Poree F, Hohne M, Gunter M, Trethewey R, Kamlage B, Poorter H, Stitt M (2008) Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ 31:518–547PubMedCrossRefGoogle Scholar
  88. Vidal EA, Gutierrez RA (2008) A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol 11:521–529PubMedCrossRefGoogle Scholar
  89. Walters RG, Ibrahim DG, Horton P, Kruger NJ (2004) A mutant of Arabidopsis lacking the triose-phosphate/phosphate translocator reveals metabolic regulation of starch breakdown in the light. Plant Physiol 135:891–906PubMedPubMedCentralCrossRefGoogle Scholar
  90. Wattebled F, Dong Y, Dumez S, Delvalle D, Planchot V, Berbezy P, Vyas D, Colonna P, Chatterjee M, Ball S, D’Hulst C (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiol 138:184–195PubMedPubMedCentralCrossRefGoogle Scholar
  91. Wattebled F, Planchot V, Dong Y, Szydlowski N, Pontoire B, Devin A, Ball S, D’Hulst C (2008) Further evidence for the mandatory nature of polysaccharide debranching for the aggregation of semicrystalline starch and for overlapping functions of debranching enzymes in Arabidopsis leaves. Plant Physiol 148:1309–1323PubMedPubMedCentralCrossRefGoogle Scholar
  92. Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Groner F, Hebbeker U, Flugge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12:787–802PubMedPubMedCentralCrossRefGoogle Scholar
  93. Weber AP, Schneidereit J, Voll LM (2004) Using mutants to probe the in vivo function of plastid envelope membrane metabolite transporters. J Exp Bot 55:1231–1244PubMedCrossRefGoogle Scholar
  94. Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD (2006) Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiol 141:879–886PubMedPubMedCentralCrossRefGoogle Scholar
  95. Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18:2971–2984PubMedPubMedCentralCrossRefGoogle Scholar
  96. Weselake RJ, Taylor DC, Rahman MH, Shah S, Laroche A, McVetty PB, Harwood JL (2009) Increasing the flow of carbon into seed oil. Biotechnol Adv 27:866–878PubMedCrossRefGoogle Scholar
  97. West M, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6:1731–1745PubMedPubMedCentralCrossRefGoogle Scholar
  98. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182PubMedCrossRefGoogle Scholar
  99. Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M, Lunn JE (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65:1051–1068PubMedPubMedCentralCrossRefGoogle Scholar
  100. Yu TS, Zeeman SC, Thorneycroft D, Fulton DC, Dunstan H, Lue WL, Hegemann B, Tung SY, Umemoto T, Chapple A, Tsai DL, Wang SM, Smith AM, Chen J, Smith SM (2005) alpha-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280:9773–9779PubMedCrossRefGoogle Scholar
  101. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004) Plastidial alpha-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135:849–858PubMedPubMedCentralCrossRefGoogle Scholar
  102. Zhang X, Myers AM, James MG (2005) Mutations affecting starch synthase III in Arabidopsis alter leaf starch structure and increase the rate of starch synthesis. Plant Physiol 138:663–674PubMedPubMedCentralCrossRefGoogle Scholar
  103. Zhang X, Szydlowski N, Delvalle D, D’Hulst C, James MG, Myers AM (2008) Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol 8:96PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Seth O’Conner
    • 1
    • 2
  • Andrea Neudorf
    • 2
  • Wenguang Zheng
    • 2
  • Mingsheng Qi
    • 3
  • Xuefeng Zhao
    • 4
  • Chuanlong Du
    • 5
  • Dan Nettleton
    • 5
  • Ling Li
    • 1
    • 2
  1. 1.Department of Biological SciencesMississippi State UniversityStarkvilleUSA
  2. 2.Department of Genetics, Development and Cell BiologyIowa State UniversityAmesUSA
  3. 3.Department of Plant Pathology and MicrobiologyIowa State UniversityAmesUSA
  4. 4.Laurence H. Baker Center for Bioinformatics and Biological StatisticsIowa State UniversityAmesUSA
  5. 5.Department of StatisticsIowa State UniversityAmesUSA

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