Skip to main content
Log in

Transgenic Turfgrasses Expressing Hyperactive Ser599Ala Phytochrome A Mutant Exhibit Abiotic Stress Tolerance

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Turfgrasses are environmentally and recreationally valuable plants that are constantly subjected to various forms of stress in their artificial and natural habitats. Previously, it was shown that the transformation of a hyperactive mutant (Serine 599 Alanine, S599A) of oat phytochrome A in zoysia grass (Zoysia japonica) and creeping bentgrass (Agrostis stolonifera L.) resulted in superior quality turfgrass with improved shade tolerance response. We now examined the abiotic stress response of the transgenic turfgrasses expressing the hyperactive mutant S599A-PhyA. The transgenic S599A-PhyA plants subjected to high salinity and heavy metal toxicity stress exhibited higher chlorophyll content, lower hydrogen peroxide level, and higher proline accumulation than the controls. Furthermore, the anti-oxidative activities of four reactive oxygen species scavenging enzymes and the total biomass (above and below-ground) were higher in S599A-PhyA plants than in the controls under both the stress conditions. Moreover, higher photosynthetic efficiency (F v/F m) of S599A-PhyA plants indicated healthier growth than the controls under stress conditions. Results suggest that the hyperactive mutant of oat phytochrome A confers abiotic stress tolerance in plants, and can be used to efficiently develop abiotic stress tolerant crops in future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ábrahám E, Hourton-Cabassa C, Erdei L, Szabados L (2010) Methods for determination of proline in plants. In: Sunkar R (ed) Plant stress tolerance: methods and protocols. Humana Press, New York, pp 317–331

    Chapter  Google Scholar 

  • Arshi A, Abdin MZ, Iqbal M (2006) Effect of CaCl2 on growth performance, photosynthetic efficiency and nitrogen assimilation of Cichorium intybus L. grown under NaCl stress. Acta Physiol Plant 28:137–147

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Bae TW, Vanjildorj E, Song SY, Nishiguchi S, Yang SS, Song IJ, Chandrasekhar T, Kang TW, Kim JI, Koh YJ, Park SY, Lee J, Lee YE, Ryu KH, Riu KZ, Song PS, Lee HY (2008) Environmental risk assessment of genetically engineered herbicide-tolerant Zoysia japonica. J Environ Qual 37:207–218

    Article  CAS  PubMed  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence at 77 K among vascular plants of diverse origins. Planta 170:489–504

    Article  PubMed  Google Scholar 

  • Boccalandro HE, Rugnone ML, Moreno JE, Ploschuk EL, Serna L, Yanovsky MJ, Casal JJ (2009) Phytochrome B enhances photosynthesis at the expense of water-use-efficiency in Arabidopsis. Plant Physiol 150:1083–1092

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Briantais JM, Dacosta JG, Ducruet JM, Moya I (1996) Heat stress induces in leaves an increase of the minimum level of chlorophyll fluorescence F0: a time-resolved analysis. Photosynth Res 48:189–196

    Article  CAS  PubMed  Google Scholar 

  • Carvalho RF, Campos ML, Azevedo RA (2011) The role of phytochrome in stress tolerance. J Integr Plant Biol 53:920–929

    Article  CAS  PubMed  Google Scholar 

  • Cheeseman JM (2006) Hydrogen peroxide concentrations in leaves under natural conditions. J Exp Bot 57:2435–2444

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  CAS  PubMed  Google Scholar 

  • de Ronde JA, Cress WA, Kruger GHJ, Strasser RJ, van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. J Plant Physiol 161:1211–1224

    Article  PubMed  Google Scholar 

  • Dobrá J, Vanková R, Havlová M, Burman AJ, Libus J, Storchova H (2011) Tobacco leaves and roots differ in the expression of proline metabolism-related genes in the course of drought stress and subsequent recovery. J Plant Physiol 168:1588–1597

    Article  PubMed  Google Scholar 

  • Elavarthi S, Bjorn M (2010) Spectrophotometric assays for antioxidant enzymes in plants. In: Sunkar R (ed) Plant stress tolerance: methods and protocols. Humana Press, New York, pp 273–280

    Chapter  Google Scholar 

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ganesan M, Han YJ, Bae TW, Hwang OJ, Chandrasekhar T, Shin AY, Goh CH, Nishiguchi S, Song IJ, Lee HY, Kim JI, Song PS (2012) Overexpression of phytochrome A and its hyperactive mutant improves shade tolerance and turf quality in creeping bentgrass and zoysiagrass. Planta 236:1135–1150

    Article  CAS  PubMed  Google Scholar 

  • Garg AK, Sawers RJH, Wang H, Kim JK, Walker JM, Brutnell TP, Parthasarathy MV, Vierstra RD, Wu RJ (2006) Light-regulated overexpression of an Arabidopsis phytochrome A gene alters plant architecture and increases grain yield. Planta 223:627–636

    Article  CAS  PubMed  Google Scholar 

  • Glombitza S, Dubuis PH, Thulke O, Welzl G, Bovet L, Götz M, Affenzeller M, Geist B, Hehn A, Asnaghi C, Ernst D, Seidlitz HK, Gundlach H, Mayer KF, Martinoia E, Werck-Reichhart D, Mauch F, Schäffner AR (2004) Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant Mol Biol 54:817–835

    Article  CAS  PubMed  Google Scholar 

  • Gupta SK, Sharma S, Santisree P, Kilambi HV, Appenroth K, Sreelakshmi Y, Sharma R (2014) Complex and shifting interactions of phytochromes regulate fruit development in tomato. Plant Cell Environ. doi:10.1111/pce.12279

    PubMed  Google Scholar 

  • Gururani MA, Upadhyaya CP, Strasser RJ, Yu JW, Park SW (2012) Physiological and biochemical responses of transgenic potato plants with altered expression of PSII manganese stabilizing protein. Plant Physiol Biochem 58:182–194

    Article  CAS  PubMed  Google Scholar 

  • Gururani MA, Upadhyaya CP, Strasser RJ, Yu JW, Park SW (2013a) Evaluation of abiotic stress tolerance in transgenic potato plants with reduced expression of PSII manganese stabilizing protein. Plant Sci 198:7–16

    Article  CAS  PubMed  Google Scholar 

  • Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park SW (2013b) Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J Plant Growth Regul 32:245–258

    Article  CAS  Google Scholar 

  • Gururani MA, Ganesan M, Song PS (2014) Photo-biotechnology as a tool to improve agronomic traits in crops. Biotech Adv 10.1016/j.biotechadv.2014.12.005

  • Holefors A, Xue ZT, Zhu LH, Welander M (2000) The Arabidopsis phytochrome B gene influences growth of the apple rootstock M26. Plant Cell Rep 19:1049–1056

    Article  CAS  Google Scholar 

  • Holst-Jensen A (2009) Testing for genetically modified organisms (GMOs): past, present and future perspectives. Biotechnol Adv 27:1071–1082

    Article  CAS  PubMed  Google Scholar 

  • Indorf M, Cordero J, Neuhaus G, Rodriguez-Franco M (2007) Salt tolerance (STO), a stress-related protein, has a major role in light signaling. Plant J 51:563–574

    Article  CAS  PubMed  Google Scholar 

  • Jang SJ, Wi SJ, Choi YJ, An G, Park KY (2012) Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: t-DNA mutational analysis of Oryza sativa lysine decarboxylase-like protein. Mol Cell 34:251–262

    Article  CAS  Google Scholar 

  • Kraepiel Y, Jullien M, Cordonnier-Pratt MM, Pratt L (1994) Identification of two loci involved in phytochrome expression in Nicotiana plumbaginifolia and lethality of the corresponding double mutant. Mol Genet Genomics 242:559–565

    Article  CAS  Google Scholar 

  • Kreslavski VD, Zorina AA, Los DA, Fomina IR, Allakhverdiev SI (2013) Molecular mechanisms of stress resistance of photosynthetic machinery. In: Rout GR, Das AB (eds) Molecular stress physiology of plants. Springer India

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Mathur S, Jajoo A, Mehta P, Bharti S (2011) Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). Plant Biol 13:1–6

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • McElwain EF, Bohnert HJ, Thomas JC (1992) Light moderates the induction of phosphoenolpyruvate carboxylase by NaCl and abscisic acid in Mesembryanthemum crystallinum. Plant Physiol 99:1261–1264

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342

    Article  CAS  PubMed  Google Scholar 

  • Orozco-Cárdenas ML, Ryan C (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557

    Article  PubMed Central  PubMed  Google Scholar 

  • Qian YL, Engelke MC, Foster MJV (2000) Salinity effects on zoysiagrass cultivars and experimental lines. Crop Sci 40:488–492

    Article  Google Scholar 

  • Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50:2–18

    Article  CAS  PubMed  Google Scholar 

  • Sinclair TR, Purcell LC, Sneller CH (2004) Crop transformation and the challenge to increase yield potential. Trends Plant Sci 9:70–75

    Article  CAS  PubMed  Google Scholar 

  • Slocombe SP, Whitelara GC, Cockburn W (1993) Investigation of phosphoenolpyruvate carboxylase (PEP carboxylasease) in Mesembryanthemum crystallinum L. in C3 and CAM photosynthetic states. Plant Cell Environ 16:403–411

    Article  CAS  Google Scholar 

  • Thomsen B, Drumm-Herrel H, Mohr H (1992) Control of the appearance of ascorbate peroxidase (EC 1.11.1.11) in mustard seedling cotyledons by phytochrome and photooxidative treatments. Planta 186:600–608

    Article  CAS  PubMed  Google Scholar 

  • Upadhyaya CP, Venkatesh J, Gururani MA, Asnin L, Sharma K, Ajappala H, Park SW (2011) Transgenic potato overproducing L-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol Lett 33:2297–2307

    Article  CAS  PubMed  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  CAS  PubMed  Google Scholar 

  • Warnke S (2003) Creeping bentgrass (Agrostis stolonifera L.). In: Casler DD, Duncan RR (eds) Turfgrass biology, genetics, and breeding. Wiley, Hoboken, pp 175–185

    Google Scholar 

  • Xie Y, Xu S, Han B, Wu M, Yuan X, Han Y, Gu Q, Xu D, Yang Q, Shen W (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Li X, Zhang L (2013) The effect of calcium chloride on growth, photosynthesis, and antioxidant responses of Zoysia japonica under drought conditions. PLoS One 8:e68214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang JC, Li M, Xie XZ, Han GL, Sui N, Wang BS (2013) Deficiency of phytochrome B alleviates chilling-induced photoinhibition in rice. Am J Bot 100:1860–1870

    Article  PubMed  Google Scholar 

  • Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee SNB (2010) Overexpression of y-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta 1797:1428–1438

    Article  CAS  PubMed  Google Scholar 

  • Zhong S, Zhao M, Shi T, Shi H, An F, Zhao Q, Guo H (2009) EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc Natl Acad Sci USA 106:21431–21436

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546

    Article  CAS  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Kalaji HM (2014) Photosynthetic responses of sun-and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynth Res 119:339–354

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Żurek G, Rybka K, Pogrzeba M, Krzyżak J, Prokopiuk K (2014) Chlorophyll a fluorescence in evaluation of the effect of heavy metal soil contamination on perennial grasses. PLoS One 9:e91475. doi:10.1371/journal.pone.0091475

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (Grant No. 2012R1A1A2000706 to PSS, Grant No. 2014R1A1A2057739 to JIK), and Next-Generation Biogreen 21 Program, Rural Development Administration, Korea (Grant No. PJ009499012014 to HYL).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pill-Soon Song.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gururani, M.A., Ganesan, M., Song, IJ. et al. Transgenic Turfgrasses Expressing Hyperactive Ser599Ala Phytochrome A Mutant Exhibit Abiotic Stress Tolerance. J Plant Growth Regul 35, 11–21 (2016). https://doi.org/10.1007/s00344-015-9502-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-015-9502-0

Keywords

Navigation