Abstract
This work aimed to evaluate the drought tolerance of transformed plants of the cultivar BRSMG Curinga that overexpress the rice phospholipase D α1 (OsPLDα1) gene. The productivity of independent transformation event plants of the OsPLDα1 gene was evaluated in an experiment where 19 days of water deficit were applied at the reproductive stage, a very strict growing condition for upland rice. The non-genetically modified cultivar (NGM) under drought treatment reduced productivity by 89% compared with that under irrigated treatment, whereas transformed plants (PLDα1_E2) reduced productivity by only 41%. After the drought treatment, the PLDα1_E2 plants productivity was five times greater than that of the NGM plant. Moreover, no adverse effects on growth and development of the transgenic plants were observed. Seven days after the resumption of irrigation, PLDα1_E2 plants had higher stomatal conductance, greater photosynthetic rate, and transpiration rate than did NGM plants, as well as a higher expression level of the OsPLDα1 gene. A delay in the senescence process was observed in these PLDα1_E2 plants, and this was determined for the recovery of photosynthesis, with greater expression of the Rubisco and lower expression of the SOD. This finding was suggestive of decreased oxidative stress, probably due to gas exchange by the partial closure of the stomata of these transformed plants, which prevented the formation of reactive oxygen species. OsPLDα1 gene overexpression resulted in a reduction in production loss under severe water deficit and revealed a possibility for the development of upland rice cultivars that are more tolerant to extreme drought conditions.
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References
Abdelrahman M, El-Sayed M, Jogaiah S, Burritt DJ, Tran P (2017) The “STAY-GREEN” trait and phytohormone signaling networks in plants under heat stress. Plant Cell Rep 36:1009–1025. https://doi.org/10.1007/s00299-017-2119-y
Arve LE, Torre S, Olsen JE, Tanino KK (2011) Stomatal responses to drought stress and air humidity, abiotic stress in plants - mechanisms and adaptations. Prof. Arun Shanker (ed), InTech. https://doi.org/10.5772/24661. Available from: https://www.intechopen.com/books/abiotic-stress-in-plants-mechanisms-and-adaptations/stomatal-responses-to-drought-stress-and-air-humidity
Ben Saad R, Fabre D, Mieulet D, Meynard D, Dingkuhn M, Al-Doss A, Guiderdoni E, Hassairi A (2012) Expression of the Aeluropus littoralis AlSAP gene in rice confers broad tolerance to abiotic stresses through maintenance of photosynthesis. Plant Cell Environ 35:626–643. https://doi.org/10.1111/j.1365-3040.2011.02441.x
Brondani C, Rangel PHN, Brondani RPV, Ferreira ME (2002) QTL mapping and introgression of yield-related traits from O. Glumaepatula to cultivated rice (Oryza sativa) using microsatellite markers. Theor Appl Genet 104:1192–1203. https://doi.org/10.1007/s00122-002-0869-5
Chen H, Yu X, Zhang X, Yang L, Huang X, Zhang J, Pritchard HW, Li W (2017) Phospholipase Dα1-mediated phosphatidic acid change is a key determinant of desiccation-induced viability loss in seeds. Plant Cell Environ 41:50–63. https://doi.org/10.1111/pce.12925
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867. https://doi.org/10.1111/tpj.13299
Counce PA, Keisling TC, Mitchell AJ (2000) A uniform, objective, and adaptive system for expressing rice development. Crop Sci 40:436–443. https://doi.org/10.2135/cropsci2000.402436x
Dedicova B, Bermudez C, Prias M, Zuniga E, Brondani C (2015) High-throughput transformation pipeline for a Brazilian japonica rice with bar gene selection. Protoplasma 252:1071–1083. https://doi.org/10.1007/s00709-014-0741-x
Dixit S, Huang BE, Sta Cruz MT, Maturan PT, Ontoy JCE, Kumar A (2014) QTLs for tolerance of drought and breeding for tolerance of abiotic and biotic stress: an integrated approach. PLoS One 9:e109574. https://doi.org/10.1371/journal.pone.0109574
Fageria NK, Wander AE, Silva SC (2014) Rice (Oryza sativa) cultivation in Brazil. Indian J Agron 59:350–358
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8(1147). https://doi.org/10.3389/fpls.2017.01147
Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase Dα retards abscisic acid- and ethylene-promoted senescence of post-harvest. Plant Cell 9:2183–2196
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212. https://doi.org/10.1051/agro:2008021
Fedoroff NV, Battisti DS, Beachy RN, Cooper PJM, Fischhoff DA, Hodges CN, Knauf VC, Lobell D, Mazur BJ, Molden D, Reynolds MP, Ronald PC, Rosegrant MW, Sanchez PA, Vonshak A, Zhu JK (2010) Radically rethinking agriculture for the 21st century. Science 327:833–834. https://doi.org/10.1126/science.1186834
Fedorova E, Zink D (2008) Nuclear architecture and gene regulation. Biochim Biophys Acta 1783:2174–2184
Gaudin AC, Henry A, Sparks AH, Slamet-Loedin IH (2013) Taking transgenic rice drought screening to the field. J Exp Bot 64:109–117. https://doi.org/10.1093/jxb/ers313
Grandjean M, Girod PA, Calabrese D, Kostyrko K, Wicht M, Yerly F, Mazza C, Beckmann JS, Martinet D, Mermod N (2011) High-level transgene expression by homologous recombination-mediated gene transfer. Nucleic Acids Res 39:e104. https://doi.org/10.1093/nar/gkr436
Gregersen PL, Culetic A, Boschian L, Krupinska K (2013) Plant senescence and crop productivity. Plant Mol Biol 82:603–622. https://doi.org/10.1007/s11103-013-0013-8
Heinemann AB, Barrios-Perez C, Ramirez-Villegas J, Arango-Londoño D, Bonilla-Findji O, Medeiros JC, Jarvis A (2015) Variation and impact of drought-stress patterns across upland rice target population of environments in Brazil. J Exp Bot 66:3625–3638. https://doi.org/10.1093/jxb/erv126
Hong Y, Zheng S, Wang X (2008) Dual functions of phospholipase Dα1 in plant response to drought. Mol Plant 1:262–269. https://doi.org/10.1093/mp/ssm025
Jagadish KS, Kavi Kishor PB, Bahuguna RN, von Wirén N, Sreenivasulu N (2015) Staying alive or going to die during terminal senescence - an enigma surrounding yield stability. Front Plant Sci 6(1070). https://doi.org/10.3389/fpls.2015.01070
Kim BR, Nam HY, Kim SU, Kim SI, Chang YJ (2003) Normalization of reverse transcription quantitative-PCR with housekeeping genes in rice. Biotechnol Lett 25:1869–1872
Kohli A, Melendi PG, Abranches R, Capell T, Stoger E, Christou P (2006) The quest to understand the basis and mechanisms that control expression of introduced transgenes in crop plants. Plant Signal Behav 1:185–195
Kumar A, Tripathi P, Singh AK (2006) Effect of dry spell on growth, development and yield of rice (Oryza sativa). Indian J Agr Sci 76:47–49
Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. J Exp Bot 65:6265–6278. https://doi.org/10.1093/jxb/eru363
Li M, Hong Y, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta 1791:927–935. https://doi.org/10.1016/j.bbalip.2009.02.017
Lu S, Bahn SC, Qu G, Qin H, Hong Y, Xu Q, Zhou Y, Hong Y, Wang X (2013) Increased expression of phospholipase Dα1 in guard cells decreases water loss with improved seed production under drought in Brassica napus. Plant Biotechnol 11:380–389. https://doi.org/10.1111/pbi.12028
Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312:264–266. https://doi.org/10.1126/science.1123769
Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP (2014) Response of plants to water stress. Front Plant Sci 5(86). https://doi.org/10.3389/fpls.2014.00086
Pantalião GF, Narciso M, Guimarães C, Castro A, Colombari JM, Breseghello F, Rodrigues L, Vianello RP, Borba TC, Brondani C (2016) Genome wide association study (GWAS) for grain yield in rice cultivated under water deficit. Genetica 144:651–664. https://doi.org/10.1007/s10709-016-9932-z
Peng Y, Zhang J, Cao G, Xie Y, Liu X, Lu M, Wang G (2010) Overexpression of a PLDα1 gene from Setaria italica enhances the sensitivity of Arabidopsis to abscisic acid and improves its drought tolerance. Plant Cell Rep 29:793–802. https://doi.org/10.1007/s00299-010-0865-1
Rebetzke GJ, Jimenez-Berni JA, Bovill WD, Deery DM, James RA (2016) High-throughput phenotyping technologies allow accurate selection of stay-green. J Exp Bot 67:4919–4924. https://doi.org/10.1093/jxb/erw301
Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, Hoff MJ, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:e45. https://doi.org/10.1093/nar/gkp045
Schapendonk AHCM, Spitters CJT, Groot PJ (1989) Effects of water stress on photosynthesis and chlorophyll fluorescence of five potato cultivars. Potato Res 32:17–32. https://doi.org/10.1007/BF02365814
Seiler C, Harshavardhan VT, Reddy PS, Hensel G, Kumlehn J, Eschen-Lippold L, Rajesh K, Korzun V, Wobus U, Lee J, Selvaraj G, Sreenivasulu N (2014) Abscisic acid flux alterations result in differential abscisic acid signaling responses and impact assimilation efficiency in barley under terminal drought stress. Plant Physiol 164:1677–1696. https://doi.org/10.1104/pp.113.229062
Serraj R, Kumar A, McNally KL, Slamet-Loedin I, Bruskiewich R, Mauleon R, Cairns J, Hijmans RJ (2009) Improvement of drought resistance in rice. Adv Agron 103:41–99. https://doi.org/10.1016/S0065-2113(09)03002-8
Serraj R, McNally KL, Slamet-Loedin I, Kohli A, Haefele SM, Atlin G, Kumar A (2011) Drought resistance improvement in rice: an integrated genetic and resource management strategy. Plant Prod Sci 14:1–14. https://doi.org/10.1626/pps.14.1
Singh A, Pandey A, Baranwal V, Kapoor S, Pandey GK (2012) Comprehensive expression analysis of rice phospholipase D gene family during abiotic stresses and development. Plant Signal Behav 7:847–855. https://doi.org/10.4161/psb.20385
Swamy BPM, Kumar A (2013) Genomics-based precision breeding approaches to improve drought tolerance in rice. Biotechnol Adv 31:1308–1318. https://doi.org/10.1016/j.biotechadv.2013.05.004
Swamy M, Ahmed HU, Henry A et al (2013) Genetic, physiological, and gene expression analyses reveal that multiple qtl enhance yield of rice mega-variety IR64 under drought. PLoS One 8:e62795. https://doi.org/10.1371/journal.pone.0062795
Vilperte V, Agapito-Tenfen SZ, Wikmark OG, Nodari RO (2016) Levels of DNA methylation and transcript accumulation in leaves of transgenic maize varieties. Environ Sci Eur 28:29. https://doi.org/10.1186/s12302-016-0097-2
Wang J, Ding B, Guo Y, Li M, Chen S, Huang G, Xie X (2014) Overexpression of a wheat phospholipase D gene, TaPLDα, enhances tolerance to drought and osmotic stress in Arabidopsis thaliana. Planta 240:103–115. https://doi.org/10.1007/s00425-014-2066-6
Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2017) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12. https://doi.org/10.1111/ppl.12540
Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci 101:9508–9513. https://doi.org/10.1073/pnas.0402112101
Zhang JL, Liu DH, Wang ZH, Yu C, Cao JH, Wang CT, Jin D-M (2009) Expression pattern of GS3 during panicle development in rice under drought stress: quantification normalized against selected housekeeping genes in real-time PCR. Asian J Plant Sci 8:285–292. https://doi.org/10.3923/ajps.2009.285.292
Acknowledgements
The Coordination for the Improvement of Higher Education Personnel/Ministry of Education (CAPES/MEC) for the grants to FRMA, JAVO and AFV. National Council for Scientific and Technological Development (CNPq) for the grants to CB and RPV and for the financial support (482724/2010-2).
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Supplemental Table 1
Gene expression of PLDα1 (N0) in PLDα1_E1 and NGM plants in three sample collections – I (80 Days After Sowing – DAS), II (92 DAS) and III (106 DAS). D means drought treatment, I means irrigated treatment. (DOCX 15 kb)
Supplemental Table 2
Gene expression of SOD (N0) in PLDα1_E2 and PLDα1_E4 plants in three sample collections – I (80 Days After Sowing – DAS), II (92 DAS) and III (106 DAS). D means drought treatment, I means irrigated treatment. (DOCX 15 kb)
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Abreu, F.R.M., Dedicova, B., Vianello, R.P. et al. Overexpression of a phospholipase (OsPLDα1) for drought tolerance in upland rice (Oryza sativa L.). Protoplasma 255, 1751–1761 (2018). https://doi.org/10.1007/s00709-018-1265-6
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DOI: https://doi.org/10.1007/s00709-018-1265-6