Yield changes of Bt-MH63 with cry1C* or cry2A* genes compared with MH63 (Oryza sativa) under different nitrogen levels

doi:10.1016/j.fcr.2013.06.017

Field Crops Research

Volume 151, September 2013, Pages 101-106

https://doi.org/10.1016/j.fcr.2013.06.017 Get rights and content

Highlights

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Bt rice, MH63 (cry1C^*) had lower grain yield than MH63.
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Lower grain yield of MH63 (cry1C^*) was due to the poor matter translocation.
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Bt rice, MH63 (cry2A^*) had lower grain yield than MH63 under zero N application.
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Lower grain yield of MH63 (cry2A^*) was possibly due to the leaf premature aging.

Abstract

Field performance of insect-resistant transgenic rice needs to be meticulously evaluated before it is commercialized. To our knowledge, little information are available about the field performance of Bt rice with cry1C^* or cry2A^* genes under different nitrogen (N) levels. Field experiments were conducted to investigate the yield performance and yield-related traits of Bt-MH63 under three N levels (0, 150 and 195 kg N ha⁻¹). The results showed that MH63 (cry1C^*) had lower grain yield than MH63 at all N levels due to the reduced grain filling percentage. Furthermore, MH63 (cry1C^*) as compared with MH63 had lower dry matter translocation efficiency and higher reservation of soluble sugar in stem and sheath at mature at all N levels. At 0 kg N ha⁻¹, grain yield and internal N use efficiency (IE_N) of MH63 (cry2A^*) were significantly lower than those of MH63 possibly due to the leaf premature aging of MH63 (cry2A^*). In contrast, there were no significant differences in the grain yield and leaf senescence between MH63 (cry2A^*) and MH63 at 150 and 195 kg N ha⁻¹. The results indicated that the incorporation of cry1C^* or cry2A^* caused varying degrees of yield reduction in rice due to different agronomic reasons.

Introduction

Recently, breeding of insect-resistant transgenic Bt rice has made great progress. Many insect-resistant transgenic rice lines were successfully cultivated (Fujimoto et al., 1993, Datta et al., 1998, Tu et al., 2000, Chen et al., 2004, Chen et al., 2005, Tang et al., 2006). In 2009, two Bt rice lines, MH63 (cry1Ab/c) and SY63 (cry1Ab/c), were granted biosafety certificates by the Ministry of Agriculture in China. The Bacillus thuringiensis (Bt) genes were transferred into crops to increase their resistance against pests. The cry1C^* and cry2A^* genes were synthesized on the basis of wild-type cry1Ca5 and cry2Aa genes of Bt, respectively, which could be effectively expressed in rice (Chen et al., 2005, Tang et al., 2006). These genes were transferred into MH63 (Minghui63), an indica CMS (cytoplasm male sterile) restorer line in China. Bt-MH63 with cry1C^* or cry2A^* genes may become important breeding materials for insect-resistant transgenic rice in China.

Bt transgenic cultivars could have higher yields by 13–23% as compared with their non-Bt counterparts under severe insect infestation (Mungai et al., 2005). Wang et al. (2012a) found that SY63 (cry1C^*) and SY63 (cry2A^*) increased yields by near 20% compared with their counterparts SY63 [Shanyou63, produced by crossbreeding MH63 with Zhenshan97A (an elite CMS line)] when no pesticides were applied against target pests. However, under low insect conditions, no yield advantages for Bt transgenic cultivars were reported (Lauer and Wedberg, 1999, Ma and Subedi, 2005). For example, no yield differences were observed in Bt-SY63 with cry1Ab/c, cry1C^* or cry2A^* compared with their non-Bt counterparts under moderate insect conditions (Tu et al., 2000, Wang et al., 2010, Wang et al., 2012b). On the other hand, some authors found decreases in the grain yields of Bt rice. Chen et al. (2006) and Xia et al. (2010) observed a yield loss in Bt/CPTI transgenic MH86 (a restorer line) under low insect pressure. Cost in grain yield brought by transgenes may not be easily detected under severe insect infestation, and therefore studying yield performance of Bt rice under no pest infestation is an essential process to evaluate the effects of incorporation of external genes.

The insertion of external genes usually caused variations in rice, such as, reduced plant height, root length, grains per panicle and grain filling percentage, which commonly led to reductions in grain yield (Shu et al., 2002, Jiang et al., 2004, Kim et al., 2008, Xia et al., 2010, Wang et al., 2012b). Although some studies were conducted to evaluate the phenotypic variations of Bt transgenic crops, few studies have been done to examine the agronomic and physiological mechanisms of the variations.

Nitrogen (N) is essential to the formation of grain yield (Kropff et al., 1993, Lawlor, 2002), and is indispensable to the Bt protein synthesis. It has been demonstrated that concentrations of Bt protein in plant tissues were significantly correlated with concentrations of overall N (Bruns and Abel, 2003, Dong and Li, 2007, Wang et al., 2012a). Subedi and Ma (2007) found that there were no significant differences in N partitioning in different tissues of Bt transgenic maize and its non-Bt counterpart. However, Chen et al. (2004) found that Bt cotton had more vigorous N metabolism in the vegetative stage compared with its non-Bt counterpart, resulting in a reduction in boll size. Previous studies showed that the incorporation of Bt genes might affect the N metabolism of transgenic crops. However, researches about N utilization and metabolism of Bt rice were relatively few so far.

The objectives of this study were (1) to investigate yield performance of Bt-MH63 with cry1C^* or cry2A^* genes compared with MH63 under different N levels and (2) to find out the main agronomic and physiological mechanisms of the yield changes.

Section snippets

Materials and methods

Three varieties, MH63 (cry1C^*), MH63 (cry2A^*) and their non-transgenic counterpart MH63 were used in the study. The cry1C^* and cry2A^* protein contents were about 2.0 and 14.0 μg g⁻¹ leaf fresh weight in Bt rice, respectively (Wang et al., 2012a).

Field experiments were conducted from May to October in 2009 and 2010 at Junchuang village, Suizhou city (31°69′N 115°33′E), Hubei Province, China. The main soil properties of the experimental site were as follows: pH, 6.09; organic C, 15.93 g kg⁻¹; total

Grain yield and yield components

Grain yields of MH63 (cry1C^*) were significantly lower than those of MH63 (cry2A^*) and MH63 at all N levels in 2009 and 2010, respectively (Table 2). MH63 (cry1C^*) reduced grain yields by 16.9 and 21.0% (means of all N levels) compared with MH63 in 2009 and 2010, respectively. The lower grain yield of MH63 (cry1C^*) was mainly due to the significant lower grain filling percentage compared with MH63 (Table 2).

In both two years at 0 kg N ha⁻¹, grain yields and grain filling percentages of MH63 (cry2A^*

Discussion

In our study, MH63 (cry1C^*) had lower grain yield than MH63, and the yield reduction was mainly ascribed to the reduced grain filling percentage (Table 2). Similarly, reduction in grain filling percentage leading to yield loss was reported in Bt rice with some other different Bt genes (Shu et al., 2002, Jiang et al., 2004, Kim et al., 2008, Xia et al., 2010). However, Wang et al. (2012b) found that Bt-SY63, produced by crossbreeding MH63 (cry1C^*) with Zhenshan97A (an elite CMS line), showed no

Acknowledgements

This study is a part of the PhD thesis research of the senior author. Funding was provided by the National Technology Project for High Food Yield of China (No. 2011BAD16B02) and National Natural Science Foundation of China (No. 31171492). We are grateful to J.M. Lenné, Co-Editor-in-Chief of Field Crops Research, for valuable suggestions. We also sincerely thank two anonymous referees for their critical comments on the original manuscript.

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However, Bt rice with high expression of Bt protein might had heavier added burden, which would be harmful to rice (Gurr and Rushton, 2005). For example, Jiang et al. (2013) found that MH63 (cry2A*) had leaf premature aging compared with MH63 when the supply of nitrogen fertilizer was inadequate. Though MH63 (cry1C*) showed a yield loss compared with MH63 under MPC in our study (Table 1), Wang et al. (2012b) found that there was no difference in grain yield between SY63 (cry1C*) and its counterpart SY63.
Transgenic Bacillus thuringiensis (Bt) rice had been successfully cultivated to maintain yield potential of rice under pest invasion. Yield and resistance performance of the transgenic Bt rice are important to be meticulously evaluated under different pest pressures. Field experiments were conducted to investigate field performances of Bt-MH63 with cry1C* or cry2A* genes under four pest control modes: chemical control for all the pests (MPC), no chemical control for the target pests (MNTP), chemical control for the target pests (MTP) and no chemical control for all the pests (MNPC). The results showed that the maximum yield advantages of MH63 (cry1C*) and MH63 (cry2A*) over MH63 were 8.4 and 25.4% (P < 0.05) under MNTP, respectively. The grain yield of MH63 (cry1C*) was lower than that of MH63 under MPC and MTP. Moreover, the grain yield of MH63 (cry2A*) was lower than that of MH63 under MTP only. The correlation analysis revealed that the yield advantages of Bt-MH63 over MH63 were positively correlated with the damage to MH63 (expressed as percentage of white leaves) caused by leaffolders (Cnaphalocrocis medinalis Guenee). Although MH63 (cry1C*) and MH63 (cry2A*) showed great differences in Bt protein contents in their leaves, they had high effective resistances to leaffolders. It can be concluded that Bt-MH63 had obvious yield advantages over MH63 when no pesticides were applied against the target pests. However, yield reductions in Bt-MH63 were existed when pesticides were applied against the target pests.

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Yield changes of Bt-MH63 with cry1C* or cry2A* genes compared with MH63 (Oryza sativa) under different nitrogen levels

Highlights

Abstract

Introduction

Section snippets

Materials and methods

Grain yield and yield components

Discussion

Acknowledgements

Field Crops Res.

Trends Biotechnol.

Field Crops Res.

Field Crops Res.

Field Crops Res.

Field Crops Res.

Field Crops Res.

Crop Prot.

Field Crops Res.

QTL-based analysis of leaf senescence in an indica/japonica hybrid in rice (Oryza sativa L.)

Theor. Appl. Genet.

Results regarding the levels of Cry1Ab protein in transgenic corn tissue (MON810) and the fate of Bt protein in the three soil types

Rom. Biotechnol. Lett.

Nitrogen-total

Nitrogen fertility effects on Bt-endotoxin and nitrogen concentrations of maize during early growth

Agron. J.

Transgenic indica rice plants harboring a synthetic cry2A* gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests

Theor. Appl. Genet.

Effects of insect-resistance genes on fecundity in rice (Oryza Sativa, Poaceae): a test for underlying cost

Am. J. Bot.

Field performance of transgenic potato plants compared with controls regenerated from tuber discs and shoot cuttings

Theor. Appl. Genet.

Constitutive and tissue-specific differential expression of the cryIA(b) gene in transgenic rice plants conferring resistance to rice insect pest

Theor. Appl. Genet.

Variability of endotoxin expression in Bt transgenic cotton

J. Agron. Crop Sci.

Insect resistant rice generated by introduction of a modified δ-endotoxin gene of Bacillus thuringiensis

Nat. Biotechnol.

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.

Standard Evaluation System for Rice

Pyramiding of insect- and disease-resistance genes into an elite indica, cytoplasm sterile restorer line of rice, Minghui63

Plant Breed.

Yield changes of Bt-MH63 with cry1C^* or cry2A^* genes compared with MH63 (Oryza sativa) under different nitrogen levels

Transgenic indica rice plants harboring a synthetic cry2A^* gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests