Abstract
Transgenic Bacillus thuringiensis (Bt) rice have been reported to acquire effective resistance against the target pests; however, the insertion and expression of alien Bt genes may have some unintended effects on the growth characteristics of rice. A screen-house experiment was conducted and repeated twice to investigate the growth characteristics and Bt protein expressions in two Bt rice lines [MH63 (Cry2A*) and MH63 (Cry1Ab/Ac)], which had different Bt protein expression levels in leaves, under zero nitrogen (N0) and recommended nitrogen (NR) fertilizer applications. Compared to the counterpart MH63, MH63 (Cry2A*) under N0 experienced accelerated leaf senescence and a lower internal N use efficiency (IEN), resulting in a 23.2% decrease in grain yield and a lower accumulated biomass. These variations were revealed to be correlated to the higher ratio of the Bt protein content to the soluble protein content (BTC/SPC) with a maximum value of 4.3‰ in MH63 (Cry2A*) leaves in the late growth stage. Under NR, no differences in growth characteristics between MH63 (Cry2A*) and MH63 were found. The growth characteristics of MH63 (Cry1Ab/Ac), with a lower BTC/SPC in the late growth stage compared to MH63 (Cry2A*), were identical to those of MH63 under the two N applications. Results show that the transgenic Bt rice MH63 (Cry2A*), with a relatively higher Bt protein expression in the late growth stage, had an inferior adaptation to nitrogen deficiency compared to its non-Bt counterpart. And this inferior adaptation was found to be correlated with the higher BTC/SPC in MH63 (Cry2A*) leaves in the late growth stage.
Similar content being viewed by others
Abbreviations
- AEN :
-
N agronomic efficiency
- Bt :
-
Bacillus thuringiensis
- BTC/SPC:
-
Ratio of the Bt protein content to the soluble protein content
- BTC:
-
Bt protein content
- C:
-
Carbon
- CMS:
-
Cytoplasm male sterile
- FL:
-
Flowering stage
- FS:
-
Filling stage
- IEN :
-
Internal N use efficiency
- K:
-
Potassium
- LSD:
-
Least significant difference
- MT:
-
Mid-tillering stage
- N0:
-
Zero nitrogen
- NPR:
-
Net photosynthetic rate
- NR:
-
Recommended nitrogen
- NUE:
-
N use efficiency
- P:
-
Phosphorus
- PEN :
-
N physiological efficiency
- PFPN :
-
N partial factor productivity
- PI:
-
Panicle initiation stage
- PM:
-
Plant maturity stage
- REN :
-
N recovery efficiency
- SD:
-
Standard deviation
- SPC:
-
Soluble protein content
References
Adamczyk J, Hardee D, Adams L, Sumerford D (2001) Correlating differences in larval survival and development of bollworm (Lepidoptera: Noctuidae) and fall armyworm (Lepidoptera: Noctuidae) to differential expression of Cry1A (c) δ-endotoxin in various plant parts among commercial cultivars of transgenic Bacillus thuringiensis cotton. J Econ Entomol 94:284–290
Bano A, Dorffling K, Bettin D, Hahn H (1993) Abscisic acid and cytokinins as possible root-to-shoot signals in xylem sap of rice plants in drying soil. Funct Plant Biol 20:109–115
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
Bremner JM, Mulvaney C (1982) Nitrogen—total. Methods of soil analysis. Part 2. Chemical and microbiological properties, 595–624
Bruns HA, Abel CA (2003) Nitrogen fertility effects on Bt δ-endotoxin and nitrogen concentrations of maize during early growth. Agron J 95:207–211
Chen DH, Ye GY, Yang CQ, Chen Y, Wu YK (2004) Effect after introducing Bacillus thuringiensis gene on nitrogen metabolism in cotton. Field Crop Res 87:235–244
Chen H, Tang W, Xu C, Li X, Lin Y, Zhang Q (2005) Transgenic indica rice plants harboring a synthetic cry2A* gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests. Theor Appl Genet 111:1330–1337
Chen M, Shelton A, Ye GY (2011) Insect-resistant genetically modified rice in China: from research to commercialization. Annu Rev Entomol 56:81–101
Clark BW, Phillips TA, Coats JR (2005) Environmental fate and effects of Bacillus thuringiensis (Bt) proteins from transgenic crops: a review. J Agr Food Chem 53:4643–4653
Cohen M, Gould F, Bentur J (2000) Bt rice: practical steps to sustainable use. Int Rice Res Notes 25:4–10
Dalling M, Boland G, Wilson J (1976) Relation between acid proteinase activity and redistribution of nitrogen during grain development in wheat. Funct Plant Biol 3:721–730
Dong H, Li W (2007) Variability of endotoxin expression in Bt transgenic cotton. J Agron Crop Sci 193:21–29
Fearing PL, Brown D, Vlachos D, Meghji M, Privalle L (1997) Quantitative analysis of CryIA (b) expression in Bt maize plants, tissues, and silage and stability of expression over successive generations. Mol Breeding 3:169–176
Fujimoto H, Itoh K, Yamamoto M, Kyozuka J, Shimamoto K (1993) Insect resistant rice generated by introduction of a modified δ-endotoxin gene of Bacillus thuringiensis. Nat Biotechnol 11:1151–1155
Gahakwa D, Maqbool SB, Fu X, Sudhakar D, Christou P, Kohli A (2000) Transgenic rice as a system to study the stability of transgene expression: multiple heterologous transgenes show similar behaviour in diverse genetic backgrounds. Theor Appl Genet 101:388–399
Gargallo-Garriga A, Sardans J, Pérez-Trujillo M, Rivas-Ubach A, Oravec M, Vecerova K, Urban O, Jentsch A, Kreyling J, Beierkuhnlein C (2014) Opposite metabolic responses of shoots and roots to drought. Sci Rep 4:6829
Greenplate JT (1999) Quantification of Bacillus thuringiensis insect control protein Cry1Ac over time in Bollgard cotton fruit and terminals. J Econ Entomol 92:1377–1383
Gurr SJ, Rushton PJ (2005) Engineering plants with increased disease resistance: what are we going to express? Trends Biotechnol 23:275–282
Hammond-Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotech 14:177–193
Hocking P, Meyer C (1991) Effects of CO2 enrichment and nitrogen stress on growth, and partitioning of dry matter and nitrogen in wheat and maize. Funct Plant Biol 18:339–356
Huber SC (1985) Role of potassium in photosynthesis and respiration. Potassium in agriculture, 369–396
IRRI, I (2002) Standard evaluation system for rice. International Rice Research Institute, Philippine
Jiang Y, Huang S, Cai M, Li C, Kong X, Zhang F, Mohamed I, Cao C (2013) Yield changes of Bt-MH63 with cry1C* or cry2A* genes compared with MH63 (Oryza sativa) under different nitrogen levels. Field Crop Res 151:101–106
Jiang Y, Pan S, Cai M, Li C, Zhan M, Wang J, Mohamed I, Cao C (2014) Assessment of yield advantages of Bt-MH63 with cry1C* or cry2A* genes over MH63 (Oryza sativa L.) under different pest control modes. Field Crop Res 155:153–158
Jin X, Yang G, Tan C, Zhao C (2015) Effects of nitrogen stress on the photosynthetic CO2 assimilation, chlorophyll fluorescence, and sugar-nitrogen ratio in corn. Sci Rep 5:160–166
Kim S, Kim C, Li W, Kim T, Li Y, Zaidi MA, Altosaar I (2008) Inheritance and field performance of transgenic Korean Bt rice lines resistant to rice yellow stem borer. Euphytica 164:829–839
Kota M, Daniell H, Varma S, Garczynski SF, Gould F, Moar WJ (1999) Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. P Natl Acad of Sci 96:1840–1845
Kranthi KR, Naidu S, Dhawad C, Tatwawadi A, Mate K, Patil E, Bharose A, Behere G, Wadaskar R, Kranthi S (2005) Temporal and intra-plant variability of Cry1Ac expression in Bt-cotton and its influence on the survival of the cotton bollworm, Helicoverpa armigera (Hubner) (Noctuidae: Lepidoptera). Curr Sci-Bangalore 89:291
Kropff M, Cassman K, Van Laar H, Peng S (1993) Nitrogen and yield potential of irrigated rice. Plant Soil 155:391–394
Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53:773–787
Li X, Ding C, Wang X, Liu B (2015a) Comparison of the physiological characteristics of transgenic insect-resistant cotton and conventional lines. Sci Rep 5:8739
Li Y, Zhang X, Chen X, Romeis J, Yin X, Peng Y (2015b) Consumption of Bt rice pollen containing Cry1C or Cry2A does not pose a risk to Propylea japonica (Thunberg)(Coleoptera: Coccinellidae). Sci Rep 5:7679
Lu HJ, Zhou XR, Gong ZX, Upadhyaya NM (2001) Generation of selectable marker-free transgenic rice using double right-border (DRB) binary vectors. Funct Plant Biol 28:241–248
Ma B, Subedi K (2005) Development, yield, grain moisture and nitrogen uptake of Bt corn hybrids and their conventional near-isolines. Field Crop Res 93:199–211
Ma C, Rui Y, Liu S, Li X, Xing B, Liu L (2015) Phytotoxic mechanism of nanoparticles: destruction of chloroplasts and vascular bundles and alteration of nutrient absorption. Sci Rep 5:11618
Mae T (1997) Physiological nitrogen efficiency in rice: nitrogen utilization, photosynthesis, and yield potential. Plant and Soil 196:201–210
Marrelli MT, Moreira CK, Kelly D, Alphey L, Jacobs-Lorena M (2006) Mosquito transgenesis: what is the fitness cost? Trends Parasitol 22:197–202
Michelmore RW (2003) The impact zone: genomics and breeding for durable disease resistance. Curr Opin Plant Biol 6:397–404
Novoa R, Loomis R (1981) Nitrogen and plant production. Plan Soil 58:177–204
Olsen K, Daly J, Holt H, Finnegan E (2005) Season-long variation in expression of Cry1Ac gene and efficacy of Bacillus thuringiensis toxin in transgenic cotton against Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol 98:1007–1017
Pandi V, Babu PS, Kailasam C (2009) Prediction of damage and yield caused by rice leaffolder at different crop Periods in a susceptible rice cultivar (IR50). J Appl Entomol 122:595–599
Peng S, Buresh RJ, Huang J, Yang J, Zou Y, Zhong X, Wang G, Zhang F (2006) Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China. Field Crop Res 96:37–47
Poongothai S, Ilavarasan R, Karrunakaran C (2010) Cry 1Ac levels and biochemical variations in Bt cotton as influenced by tissue maturity and senescence. Plant Breed. Crop Sci 2:96–103
Rose MT, Rose TJ, Pariasca-Tanaka J, Wissuwa M (2011) Revisiting the role of organic acids in the bicarbonate tolerance of zinc-efficient rice genotypes. Funct Plant Biol 38:493–504
Shu QY, Cui HR, Ye GY, Wu DX, Xia YW, Gao MW, Altosaar I (2002) Agronomic and morphological characterization of Agrobacterium-transformed Bt rice plants. Euphytica 127:345–352
Siebert MW, Patterson T, Gilles G, Nolting S, Braxton L, Leonard B, Van Duyn J, Lassiter R (2009) Quantification of Cry1Ac and Cry1F Bacillus thuringiensis insecticidal proteins in selected transgenic cotton plant tissue types. J Econ Entomol 102:1301–1308
Subedi K, Ma B (2007) Dry matter and nitrogen partitioning patterns in Bt and non-Bt near-isoline maize hybrids. Crop Sci 47:1186–1192
Sun C, Zhang L, Wu Q, Miao L, Wang G, Li S (2007) Nitrogen metabolism of transgenic Bt cotton and transgenic Bt CpTI cotton at seedling stage. Chin J Ecol 26:187–191
Tang W, Chen H, Xu C, Li X, Lin Y, Zhang Q (2006) Development of insect-resistant transgenic indica rice with a synthetic cry1C* gene. Mol Breed 18:1–10
Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2015) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 5:12449
Tu J, Datta K, Alam MF, Fan Y, Khush GS, Datta SK (1998) Expression and function of a hybrid Bt toxin gene in transgenic rice conferring resistance to insect pest. Plant Biotechnol 15:195–203
Tu J, Datta K, Khush G, Zhang Q, Datta S (2000a) Field performance of Xa21 transgenic indica rice (Oryza sativa L.), IR72. Theor Appl Genet 101:15–20
Tu J, Zhang G, Datta K, Xu C, He Y, Zhang Q, Khush GS, Datta SK (2000b) Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensis δ-endotoxin. Nat Biotechnol 18:1101–1104
Wang F, Jian Z, Nie L, Cui K, Peng S, Lin Y, Huang J (2012a) Effects of N treatments on the yield advantage of Bt-SY63 over SY63 (Oryza sativa) and the concentration of Bt protein. Field Crop Res 129:39–45
Wang F, Ye C, Zhu L, Nie L, Cui K, Peng S, Lin Y, Huang J (2012b) Yield differences between Bt transgenic rice lines and their non-Bt counterparts, and its possible mechanism. Field Crop Res 126:8–15
Wei-Dong Y, Wei-Ming S, Bao-Hai L, Zhang M (2007) Overexpression of a foreign Bt gene in cotton affects the low-molecular-weight components in root exudates. Pedosphere 17:324–330
Xia H, Chen L, Wang F, Lu BR (2010) Yield benefit and underlying cost of insect-resistance transgenic rice: implication in breeding and deploying transgenic crops. Field Crop Res 118:215–220
Yamaya T, Obara M, Nakajima H, Sasaki S, Hayakawa T, Sato T (2002) Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. J Exp Bot 53:917–925
Yu H, Xu X, Yuan B, Hui W, Liu FZ, Wang MQ, Gang W, Hua HX (2011) The influence of transgenic cry1Ab/cry1Ac, cry1C and cry2A rice on non-target planthoppers and their main predators under field conditions. Agr Sci China 10:1739–1747
Yuan Y, Xu W, He X, Liu H, Cao S, Qi X, Huang K, Luo Y (2013) Effects of genetically modified T2A–1 rice on the GI health of rats after 90-day supplement. Sci Rep 3:1962
Yukui R, Wenya W, Pinghui L, Fusuo Z (2009) Mineral element distribution in organs of dual-toxin transgenic (Bt+ CpTI) cotton seedling. Plant Biosyst 143:137–139
Zhang Z, Tian X, Duan L, Wang B, He Z, Li Z (2007) Differential responses of conventional and Bt-transgenic cotton to potassium deficiency. J Plant Nutr 30:659–670
Acknowledgements
We express our gratitude to the National Key Laboratory of Crop Genetic Improvement for providing the seeds of MH63 (Cry2A*) and MH63 (Cry1Ab/Ac). This work was funded by the National Natural Science Foundation of China (No. 31371570).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The Authors declare that they have no conflict of interest.
Additional information
Communicated by Z.-L. Zhang.
Electronic supplementary material
Below is the link to the electronic supplementary material.
11738_2017_2384_MOESM1_ESM.tif
Fig. S1 Total N uptakes of Bt-MH63 and MH63 under different N applications in 2012 and 2013. Lowercase letters indicate LSD (α=0.05) grouping of means across genotypes within an N application for each year. Columns with the same letter are not significantly different. The vertical bars indicate standard deviations (TIFF 1082 kb)
11738_2017_2384_MOESM2_ESM.jpg
Fig. S2 Pot experiment in the screen-house at Huazhong Agricultural University, Wuhan City (29°58′N 113°53′E), Hubei Province, China (JPEG 3341 kb)
Rights and permissions
About this article
Cite this article
Jiang, Y., Ling, L., Zhang, L. et al. Different response of an elite Bt restorer line of hybrid rice (Oryza sativa L.) in adaptation to nitrogen deficiency. Acta Physiol Plant 39, 89 (2017). https://doi.org/10.1007/s11738-017-2384-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-017-2384-y