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Adaptive responses of amino acid metabolism to the combination of desiccation and low nitrogen availability in Sporobolus stapfianus

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Abstract

Main conclusion

Depending on nitrogen availability, S. stapfianus uses different amino acid metabolism strategies to cope with desiccation stress. The different metabolic strategies support essential processes for the desiccation tolerance phenotype.

To provide a comprehensive assessment of the role played by amino acids in the adaptation of Sporobolus stapfianus to a combination of desiccation and nitrogen limitation, we used an absolute quantification of free and protein-bound amino acids (FAAs and PBAAs) as well as their gamma-glutamyl (gg-AA) derivatives in four different tissues grown under high- and low-nitrogen regimes. We demonstrate that although specific FAAs and gg-AAs increased in desiccating immature leaves under both nitrogen regimes, the absolute change in the total amount of either is small or negligible, negating their proposed role in nitrogen storage. FAAs and PBAAs decrease in underground tissues during desiccation, when nitrogen is abundant. In contrast, PBAAs are drastically reduced from the mature leaves, when nitrogen is limiting. Nevertheless, the substantial reduction in PBAA and FAA fractions in both treatments is not manifested in the immature leaves, which strongly suggests that these amino acids are further metabolized to fuel central metabolism or other metabolic adjustments that are essential for the acquisition of desiccation tolerance (DT).

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Abbreviations

(T)FAAs:

(Total) free amino acids

(T)PBAAs:

(Total) protein-bound amino acids

(T)gg-AAs:

(Total) gamma-glutamyl amino acids

DS:

Desiccation sensitive

DT:

Desiccation tolerance

References

  • Angelovici R, Lipka AE, Deason N, Gonzalez-Jorge S, Lin H, Cepela J, Buell R, Gore MA, Dellapenna D (2013) Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. Plant Cell 25(12):4827–4843. https://doi.org/10.1105/tpc.113.119370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arakawa T, Timasheff SN (1985) Theory of protein solubility. Methods Enzymol 114:49–77

    Article  CAS  Google Scholar 

  • Arakawa T, Kita Y, Carpenter JF (1991) Protein–solvent interactions in pharmaceutical formulations. Pharm Res 8(3):285–291

    Article  CAS  Google Scholar 

  • Avice JC, Le Dily F, Goulas E, Noquet C, Meuriot F, Volenec JJ, Cunningham SM, Sors TG, Dhont C, Castonguay Y, Nadeau P, Bélanger G, Chalifour FP, Ourry A (2003) Vegetative storage proteins in overwintering storage organs of forage legumes: roles and regulation. Can J Bot 81(12):1198–1212. https://doi.org/10.1139/b03-122

    Article  CAS  Google Scholar 

  • Bausenwein U, Millard P, Raven JA (2001) Remobilized old-leaf nitrogen predominates for spring growth in two temperate grasses. New Phytol 152(2):283–290. https://doi.org/10.1046/j.0028-646X.2001.00262.x

    Article  Google Scholar 

  • Blomstedt CK, Gianello RD, Hamill JD, Neale AD, Gaff DF (1998) Drought-stimulated genes correlated with desiccation tolerance of the resurrection grass Sporobolus stapfianus. Plant Growth Regul 24(3):153–161

    Article  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218(4571):443–448. https://doi.org/10.1126/science.218.4571.443

    Article  CAS  PubMed  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan B, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. ASPB, Rockville, pp 1158–1249

    Google Scholar 

  • Burke A (2002) Properties of soil pockets on arid Nama Karoo inselbergs—the effect of geology and derived landforms. J Arid Environ 50(2):219–234

    Article  Google Scholar 

  • Dalla Vecchia F, El Asmar T, Calamassi R, Rascio N, Vazzana C (1998) Morphological and ultrastructural aspects of dehydration and rehydration in leaves of Sporobolus stapfianus. Plant Growth Regul 24(3):219–228

    Article  CAS  Google Scholar 

  • Dinakar C, Bartels D (2013) Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis. Front Plant Sci 4:482. https://doi.org/10.3389/fpls.2013.00482

    Article  PubMed  PubMed Central  Google Scholar 

  • Dorrstock S, Prembski S, Barthlott W (1996) Ephemeral flush vegetation on inselbergs in the Ivory Coast (West Africa). Candollea 51:407–419

    Google Scholar 

  • Gaff DF (1977) Desiccation tolerant vascular plants of southern Africa. Oecologia 31(1):95–109. https://doi.org/10.1007/BF00348713

    Article  CAS  PubMed  Google Scholar 

  • Gaff DF, Loveys BR (1992) Abscisic acid levels in drying plants of a resurrection grass. Trans Malays Soc Plant Physiol 3:286–287

    Google Scholar 

  • Gaff DF, Oliver M (2013) The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct Plant Biol 40(4):315–328

    Article  Google Scholar 

  • Gaff DF, Blomstedt CK, Neale AD, Le TN, Hamill JD, Ghasempour HR (2009) Sporobolus stapfianus, a model desiccation-tolerant grass. Funct Plant Biol 36(7):589–599

    Article  CAS  Google Scholar 

  • Ghasempour HR, Gaff DF, Williams RPW, Gianello RD (1998) Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regul 24(3):185–191

    Article  CAS  Google Scholar 

  • Gloser V (2002) Seasonal changes of nitrogen storage compounds in a rhizomatous grass Calamagrostis epigeios. Biol Plant 45(4):563–568

    Article  CAS  Google Scholar 

  • Griffiths CA, Gaff DF, Neale AD (2014) Drying without senescence in resurrection plants. Front Plant Sci 5:36. https://doi.org/10.3389/fpls.2014.00036

    Article  PubMed  PubMed Central  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466. https://doi.org/10.4161/psb.21949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6(9):431–438

    Article  CAS  Google Scholar 

  • Ingle RA, Schmidt UG, Farrant JM, Thomson JA, Mundree SG (2007) Proteomic analysis of leaf proteins during dehydration of the resurrection plant Xerophyta viscosa. Plant Cell Environ 30(4):435–446

    Article  CAS  Google Scholar 

  • Jiang GQ, Wang Z, Shang HH, Yang WL, Hu Z, Phillips J, Deng X (2007) Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta 225(6):1405–1420

    Article  CAS  Google Scholar 

  • Kavanova M, Gloser V (2005) The use of internal nitrogen stores in the rhizomatous grass Calamagrostis epigejos during regrowth after defoliation. Ann Bot-London 95(3):457–463

    Article  CAS  Google Scholar 

  • Koenig D, Weigel D (2015) Beyond the thale: comparative genomics and genetics of Arabidopsis relatives. Nat Rev Genet 16(5):285–298. https://doi.org/10.1038/nrg3883

    Article  CAS  PubMed  Google Scholar 

  • Kramer U (2018) Conceptualizing plant systems evolution. Curr Opin Plant Biol 42:66–75. https://doi.org/10.1016/j.pbi.2018.02.008

    Article  PubMed  Google Scholar 

  • Le TN, Blomstedt CK, Kuang JB, Tenlen J, Gaff DF, Hamill JD, Neale AD (2007) Desiccation-tolerance specific gene expression in leaf tissue of the resurrection plant Sporobolus stapfianus. Funct Plant Biol 34(7):589–600

    Article  CAS  Google Scholar 

  • Martinelli T, Whittaker A, Bochicchio A, Vazzana C, Suzuki A, Masclaux-Daubresse C (2007) Amino acid pattern and glutamate metabolism during dehydration stress in the ‘resurrection’ plant Sporobolus stapfianus: a comparison between desiccation-sensitive and desiccation-tolerant leaves. J Exp Bot 58(11):3037–3046. https://doi.org/10.1093/jxb/erm161

    Article  CAS  PubMed  Google Scholar 

  • Meister A, Larsson A (1995) Glutathione synthetase deficiency and other disorders of the gamma-glutamyl cycle. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) Metabolic and molecular bases of inherited diseases, vol 1. McGraw-Hill, New York, pp 1461–1495

    Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11(1):15–19. https://doi.org/10.1016/j.tplants.2005.11.002

    Article  CAS  PubMed  Google Scholar 

  • Neale AD, Blomstedt CK, Bronson P, Le TN, Guthridge K, Evans J, Gaff DF, Hamill JD (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe drought stress. Plant Cell Environ 23(3):265–277

    Article  CAS  Google Scholar 

  • Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A gamma-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol 148(3):1603–1613. https://doi.org/10.1104/pp.108.125716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BW, Cushman JC (2011a) A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23(4):1231–1248. https://doi.org/10.1105/tpc.110.082800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver MJ, Jain R, Balbuena TS, Agrawal G, Gasulla F, Thelen JJ (2011b) Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration. Phytochemistry 72(10):1273–1284. https://doi.org/10.1016/j.phytochem.2010.10.020

    Article  CAS  PubMed  Google Scholar 

  • Peterson PM, Romaschenko K, Arrieta YH, Saarela JM (2014) A molecular phylogeny and new subgeneric classification of Sporobolus (Poaceae: Chloridoideae: Sporobolinae). Taxon 63(6):1212–1243

    Article  Google Scholar 

  • Porembski S, Barthlott W (2000) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecol 151(1):19–28

    Article  Google Scholar 

  • Quartacci MF, Forli M, Rascio N, DallaVecchia F, Bochicchio A, Navari-Izzo F (1997) Desiccation-tolerant Sporobolus stapfianus: lipid composition and cellular ultrastructure during dehydration and rehydration. J Exp Bot 48(311):1269–1279

    Article  CAS  Google Scholar 

  • Robinson PW, Hodges CF (1977) Effect of nitrogen fertilization on free amino acid and soluble sugar content of Poa pratensis and on infection and disease severity by Drechslera sorokiniana. Phytopathology 67:1239–1244

    Article  CAS  Google Scholar 

  • Sharma S, Verslues PE (2010) Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant Cell Environ 33(11):1838–1851

    Article  CAS  Google Scholar 

  • Sharma S, Villamor JG, Verslues PE (2011) Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiol 157(1):292–304

    Article  CAS  Google Scholar 

  • Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203(1):32–43. https://doi.org/10.1111/nph.12797

    Article  PubMed  Google Scholar 

  • UN (2010) United Nations 2010–2020 decade for deserts and the fight against desertification. http://www.un.org/en/events/desertification_decade/whynow.shtml

  • Volenec JJ, Ourry A, Joern BC (1996) A role for nitrogen reserves in forage regrowth and stress tolerance. Physiol Plant 97(1):185–193

    Article  CAS  Google Scholar 

  • Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S (2010) Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res 9(12):6561–6577. https://doi.org/10.1021/pr100767k

    Article  CAS  PubMed  Google Scholar 

  • Whittaker A, Bochicchio A, Vazzana C, Lindsey G, Farrant J (2001) Changes in leaf hexokinase activity and metabolite levels in response to drying in the desiccation-tolerant species Sporobolus stapfianus and Xerophyta viscosa. J Exp Bot 52(358):961–969

    Article  CAS  Google Scholar 

  • Whittaker A, Martinelli T, Farrant JM, Bochicchio A, Vazzana C (2007) Sucrose phosphate synthase activity and the co-ordination of carbon partitioning during sucrose and amino acid accumulation in desiccation-tolerant leaf material of the C4 resurrection plant Sporobolus stapfianus during dehydration. J Exp Bot 58(13):3775–3787. https://doi.org/10.1093/jxb/erm228

    Article  CAS  PubMed  Google Scholar 

  • Yobi A, Angelovici R (2018) A high-throughput absolute-level quantification of protein-bound amino acids in seeds. Curr Protoc Plant Biol. https://doi.org/10.1002/cppb.20084

    Article  PubMed  Google Scholar 

  • Yobi A, Wone BW, Xu W, Alexander DC, Guo L, Ryals JA, Oliver MJ, Cushman JC (2012) Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of Selaginella reveals insights into the resurrection trait. Plant J 72(6):983–999. https://doi.org/10.1111/tpj.12008

    Article  CAS  PubMed  Google Scholar 

  • Yobi A, Wone BW, Xu W, Alexander DC, Guo L, Ryals JA, Oliver MJ, Cushman JC (2013) Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. Mol Plant 6(2):369–385. https://doi.org/10.1093/mp/sss155

    Article  CAS  PubMed  Google Scholar 

  • Yobi A, Schlauch KA, Tillett RL, Yim WC, Espinoza C, Wone BW, Cushman JC, Oliver MJ (2017) Sporobolus stapfianus: insights into desiccation tolerance in the resurrection grasses from linking transcriptomics to metabolomics. BMC Plant Biol 17(1):67. https://doi.org/10.1186/s12870-017-1013-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zandalinas SI, Mittler R, Balfagon D, Arbona V, Gomez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162(1):2–12. https://doi.org/10.1111/ppl.12540

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Song X, Bartels D (2016) Enzymes and metabolites in carbohydrate metabolism of desiccation tolerant plants. Proteomes 4(4):40. https://doi.org/10.3390/proteomes4040040

    Article  CAS  PubMed Central  Google Scholar 

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Acknowledgements

The authors wish to acknowledge Melody Kroll for editing assistance and James Elder for technical help with tissue collection.

Funding

This study was funded in part by the National Science Foundation (NSF) 1355406 (EPSCoR; The Missouri Transect, Climate, Plants, and Community) to RA and NSF IOS-1444448 to MJO (Robert Sharp PI) and Agricultural Research Services (ARS) Project 5070-21000-038-00D for MJO. Mention of trademark or proprietary product does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products that may be suitable.

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  1. Albert Batushansky

    Present address: Aging and Metabolism Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA

Authors and Affiliations

  1. Division of Biological Sciences, Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65311, USA

    Abou Yobi, Albert Batushansky & Ruthie Angelovici

  2. U.S. Department of Agriculture-Agricultural Research Service, Plant Genetic Research Unit, University of Missouri, Columbia, MO, 65211, USA

    Melvin J. Oliver

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Correspondence to Ruthie Angelovici.

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Yobi, A., Batushansky, A., Oliver, M.J. et al. Adaptive responses of amino acid metabolism to the combination of desiccation and low nitrogen availability in Sporobolus stapfianus. Planta 249, 1535–1549 (2019). https://doi.org/10.1007/s00425-019-03105-6

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