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Overexpression of Receptor-Like Kinase ERECTA Improves Thermotolerance in Rice and Tomato

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Overexpression of Receptor-Like Kinase ERECTA Improves Thermotolerance in Rice and Tomato LETTERS Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato Hui Shen1,2,9, Xiangbin Zhong1,9, Fangfang Zhao1, Yanmei Wang1, Bingxiao Yan1, Qun Li1, Genyun Chen1, Bizeng Mao3, Jianjun Wang4, Yangsheng Li5, Guoying Xiao6, Yuke He1, Han Xiao1, Jianming Li7 & Zuhua He1,8 The detrimental effects of global warming on crop productivity Overexpression of HSP101 increased tolerance to heat shock or threaten to reduce the world’s food supply1–3. Although plant prolonged heat stress in transgenic Arabidopsis, tobacco and cot- responses to changes in temperature have been studied4, ton9,14, although transgenic cotton produced fewer bolls and seeds genetic modification of crops to improve thermotolerance than control cotton plants under normal growth conditions14. has had little success to date. Here we demonstrate that On the other hand, engineering to increase the tolerance of plants to overexpression of the Arabidopsis thaliana receptor-like high temperatures during multiple hot summer seasons at different kinase ERECTA (ER) in Arabidopsis, rice and tomato locations has not been reported. In particular, there are few confers thermotolerance independent of water loss and that reports of engineering or breeding of thermotolerant staple crop Arabidopsis er mutants are hypersensitive to heat. A loss- species, except for a recent study, which reported that natural alleles of of-function mutation of a rice ER homolog and reduced a gene encoding proteasome α2 subunit from African rice contribute expression of a tomato ER allele decreased thermotolerance of to thermotolerance15. Therefore, genes other than HSP101 are critical both species. Transgenic tomato and rice lines overexpressing to thermotolerance improvement in crops16. Arabidopsis ER showed improved heat tolerance in the The model plant Arabidopsis is sensitive to high temperatures, 17,18 greenhouse and in field tests at multiple locations in China probably owing to local adaptation , and cannot survive prolonged during several seasons. Moreover, ER-overexpressing transgenic heat stress19. Following our previous studies of Arabidopsis heat and Arabidopsis, tomato and rice plants had increased biomass. harmattan responses19–21, we report in this study that two ecotypes, Nature America, Inc. All rights reserved. America, Inc. Nature Our findings could contribute to engineering or breeding Columbia-0 (Col-0) and Landsberg erecta (Ler), were substantially dif- 5 thermotolerant crops with no growth penalty. ferent from each other in their tolerance to prolonged extreme heat in greenhouse conditions (40 °C; Fig. 1a). Ler plants began wilting 12 h © 201 The temperature increases associated with global warming reduce after transfer from 22 °C to 40 °C and completely wilted or died 48 h plant growth and crop productivity3. In particular, a harmattan climate, after heat treatment. Col-0 plants, however, only began wilting 36 h which brings desert-like conditions, causes immediate death of plants after heat treatment, and a fraction (~50%) of their leaves retained npg or their tissues. It has been estimated that rice grain yield declines osmotic pressure 48 h after heat treatment, resulting in a significantly by 10% for each 1 °C increase in local night temperature in the dry higher survival rate (47.2%) compared with Ler (7.8%) 48 h after heat season1 and that global warming has a negative impact on the yield treatment (Supplementary Fig. 1a). This difference in heat tolerance of other major grain crops including wheat, maize and barley2. indicates that the Col-0 strain contains one or more gene(s) for heat The heat wave during the 2013 summer in eastern China had a dev- tolerance (Hat). To map Hat loci in Col-0, we first screened a set astating impact on crops. Plants respond to temperature changes by of recombinant inbred lines (RILs) derived from a cross of Col and reprogramming their growth and development4–8, and progress has Ler. These lines were classified into three groups based on survival been made towards genetic modification of plants to increase their rates: lines with high tolerance (similar to Col-0), lines with high tolerance to heat stress. However, these studies have mainly been sensitivity (similar to Ler) and lines with intermediate properties restricted to the model plant Arabidopsis9–14. Many studies have (Supplementary Fig. 1a). Based on the RIL phenotype, two major shown that expression of heat shock proteins (HSPs) can improve quantitative trait loci (QTL) were detected: qHat2-1, with a single peak the tolerance of transgenic plants to heat shock (short exposure to having an LOD score of 6.6 and 30% contribution on chromosome 2, high temperatures)15. In particular, HSP101 is required for thermo- and qHat2-2, with three small peaks with an LOD score of 5.0–6.9 tolerance in plants and has potential as a tool for crop improvements. and 23–28% contribution on chromosome 4 (Supplementary Fig. 1b 1National Key Laboratory of Plant Molecular Genetics and National Center of Plant Gene Research, Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China. 2Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai Chenshan Botanical Garden, Shanghai, China. 3College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China. 4Zhejiang Academy of Agricultural Sciences, Hangzhou, China. 5College of Life Science, Wuhan University, Hubei, China. 6Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, China. 7Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China. 8Collaborative Innovation Center of Genetics and Development, Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China. 9These authors contributed equally to this work. Correspondence should be addressed to Z.H. ([email protected]). Received 10 February; accepted 21 July; published online 17 August 2015; doi:10.1038/nbt.3321 996 VOLUME 33 NUMBER 9 SEPTEMBER 2015 NATURE BIOTECHNOLOGY LETTERS and Supplementary Table 1). We decided to fine-map the qHat2-1 whether ER is the qHat2-1 locus, we first measured the heat locus by constructing chromosome segment substitution lines sensitivity of er mutants in Col-0 and observed that a null er mutant, (CSSLs), with Ler as the recurrent parent, that cover chromosome 2 er-105 (ref. 22), was more sensitive to heat than the wild-type Col-0 with five CSSLs (Supplementary Fig. 1c). The line CSSL-2-3 was (Supplementary Fig. 2a,b). A similar difference in heat sensitivity associated with a considerably higher survival ratio compared was also observed between Ler and its wild-type Landsberg (Lan) with other CSSLs (Supplementary Fig. 1d), indicating that CSSL-2-3 (Supplementary Fig. 2c,d). We next transformed er-105 with the contains the qHat2-1 locus for heat tolerance. Col-0 wild-type ER gene driven by its native promoter (pER::ER) and The line CSSL-2-3 covers a 493-kb region of chromosome 2, and found that the pER::ER transgene completely restored heat tolerance the middle of this segment contains the ER gene (Supplementary of the null mutant (Supplementary Fig. 2a,b). Similar results were Fig. 1d), which encodes a receptor-like kinase that was mutated in obtained by complementation with the same pER::ER transgene in Ler and has been implicated in diverse growth and development Ler lines (Supplementary Fig. 2c,d). Thus, we conclude that ER is the processes22–28, including warmth-induced abnormal adaxial-abaxial functional gene for qHat2-1, and that er loss-of-function mutations polarity in leaf patterning29 and photosynthetic capacity30. To evaluate greatly reduce heat tolerance. a Heat treatment (40 °C) d e f g 0 h 12 h 24 h 36 h 48 h Markerer-105Col-0LM13LM17LM10 25 22 °C 22 °C 22 °C 170 kDa 0.5 25 ** ER-MH(α-MYC) 20 ** ** ** 130 kDa 0.4 * 20 15 100 kDa ** 0.3 15 ** 10 Col-0 0.2 10 per plant 70 kDa plant (g) ** 5 0.1 per plant (g) 5 55 kDa Seed weight per Actin 0 0 Shoot dry weight 0 Inflorescence number Col-0 L7-1 Col-0 L2-3 L7-1 Col-0 L2-3 L7-1 er-105 er-105 er-105 er L Genotype Genotype Genotype 22 °C h i j 100 b 40 °C 40 °C Col-0 ** ** Col-0 er-105 L2-3 L7-1 Col-0 L7-1 80 * * 30 °C 60 ** 40 er-105 ** ** 20 Survival rate (%) 0 L2-3 40 °C 48 h 30 °C 30 d Col-0 L2-3L7-1 Col-0 L2-3L7-1 Col-0 Col-0L7-1 er-105 er-105 er-105LM13LM17LM10 Genotype L7-1 Nature America, Inc. All rights reserved. America, Inc. Nature 22 °C 22 °C 22 °C 35S::ER 5 l ** k 5 m 3.5 ** 0.20 ** 4 3.0 © 201 * 0.15 2.5 /s) 3 c 2 2.0 30 °C Col-0 er-105 L7-1 0.10 2 1.5 * mol/mmol) µ (mol/m ( WUE (mg/g) npg 1.0 * 0.05 1 Instantaneous WUE 0.5 Stomatal conductance 0 0 0 Col-0 L7-1 Col-0 L7-1 Col-0 L7-1 Col-0 L7-1 er-105 er-105 Genotype Genotype Genotype Figure 1 ER plays an important role in heat tolerance in Arabidopsis. (a) Pictures of 2-week-old Arabidopsis plants grown in a 40 °C growth chamber for 0, 12, 24, 36 and 48 h. Scale bar, 1 cm. (b) Pictures of 4-week-old plants grown at 22 °C (left panels) of the wild-type Col-0, er-105 and two ER-OE lines (L2-3 and L7-1) and their corresponding individual leaves of different developmental stages (right panels). Scale bars, 1 cm. (c) Mature plants of Col-0, er-105 and L7-1 grown at 22 °C.
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