MdWRKY40is directly promotes anthocyanin accumulation and blocks MdMYB15L, the repressor of MdCBF2, which improves cold tolerance in apple

doi:10.1016/j.jia.2023.04.033

Journal of Integrative Agriculture

2023, Vol. 22

Issue (6): 1704-1719 DOI: 10.1016/j.jia.2023.04.033

Horticulture

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MdWRKY40is directly promotes anthocyanin accumulation and blocks MdMYB15L, the repressor of MdCBF2, which improves cold tolerance in apple

XU Peng-yue^1*, XU Li^1*, XU Hai-feng¹, HE Xiao-wen¹, HE Ping¹, CHANG Yuan-sheng¹, WANG Sen¹, ZHENG Wen-yan¹, WANG Chuan-zeng², CHEN Xin¹, LI Lin-guang^1#, WANG Hai-bo^1#

¹ Shandong Institute of Pomology, Shandong Academy of Agricultural Sciences, Tai’an 271000, P.R.China

² Modern Agriculture Research Institute of Yellow River Delta, Shandong Academy of Agricultural Sciences, Dongying 257000, P.R.China

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摘要

冷胁迫是影响苹果生产的重要限制因素。在本研究中，我们以苹果砧木‘M9T337’和‘60-160’的组织培养幼苗为试材进行检测，发现它们对冷胁迫分别表现为抗性和敏感性。‘M9T337’和‘60-160’幼苗在冷胁迫（1℃）处理48小时后，差异表达基因（DEGs）的富集途径和生理变化明显不同，表明它们对冷胁迫的反应存在差异。两个砧木幼苗WRKY转录因子差异表达分析表明MdWRKY40is和MdWRKY48为潜在冷耐性调控子。在苹果愈伤中分别过表达MdWRKY40is和MdWRKY48，结果发现过表达MdWRKY48的愈伤没有明显效果，而MdWRKY40is能促进花青苷积累和提高愈伤冷耐性，并促进花青苷合成结构基因MdDFR和冷信号核心基因MdCBF2的表达。酵母单杂和凝胶阻滞（ EMSA ）分析表明MdWRKY40is仅能结合MdDFR的启动子。酵母双杂和双分子荧光互补（BiFC）表明MdWRKY40is能通过其蛋白N端Leu Zipper与CBF2抑制子MdMYB15L互作。当敲除MdWRMY40is蛋白N端Leu Zipper后，在愈伤中过表达发现其不能影响MdCBF2的表达水平和愈伤冷耐性，表明MdWRKY40is参与冷信号途径是通过与MdMYB15L互作来实现的。综上，MdWRKY40is能直接绑定MdDFR启动子促进花青苷积累，并通过与MdMYB15L互作，干扰其对MdCBF2抑制作用，间接促进MdCBF2表达，从而提高冷耐性。这些结果为苹果砧木抗冷机制的研究提供了新视角，为未来筛选抗寒砧木提供分子依据。

Abstract

Cold stress is an important factor that limits apple production. In this study, we examined the tissue-cultured plantlets of apple rootstocks ‘M9T337’ and ‘60-160’, which are resistant and sensitive to cold stress, respectively. The enriched pathways of differentially expressed genes (DEGs) and physiological changes in ‘M9T337’ and ‘60-160’ plantlets were clearly different after cold stress (1°C) treatment for 48 h, suggesting that they have differential responses to cold stress. The differential expression of WRKY transcription factors in the two plantlets showed that MdWRKY40is and MdWRKY48 are potential regulators of cold tolerance. When we overexpressed MdWRKY40is and MdWRKY48 in apple calli, the overexpression of MdWRKY48 had no significant effect on the callus, while MdWRKY40is overexpression promoted anthocyanin accumulation, increased callus cold tolerance, and promoted the expression of anthocyanin structural gene MdDFR and cold-signaling core gene MdCBF2. Yeast one-hybrid screening and electrophoretic mobility shift assays showed that MdWRKY40is could only bind to the MdDFR promoter. Yeast two-hybrid screening and bimolecular fluorescence complementation showed that MdWRKY40is interacts with the CBF2 inhibitor MdMYB15L through the leucine zipper (LZ). When the LZ of MdWRMY40is was knocked out, MdWRKY40is overexpression in the callus did not affect MdCBF2 expression or callus cold tolerance, indicating that MdWRKY40is acts in the cold signaling pathway by interacting with MdMYB15L. In summary, MdWRKY40is can directly bind to the MdDFR promoter in order to promote anthocyanin accumulation, and it can also interact with MdMYB15L to interfere with its inhibitory effect on MdCBF2, indirectly promoting MdCBF2 expression, and thereby improving cold tolerance. These results provide a new perspective for the cold-resistance mechanism of apple rootstocks and a molecular basis for the screening of cold-resistant rootstocks.

Keywords: MdWRKY40is anthocyanin accumulation MdMYB15L MdCBF2 cold tolerance

Received: 02 December 2022 Online: 28 April 2023 Accepted: 24 March 2023

Fund:

This work was supported by the Natural Science Foundation of Shandong Province, China (ZR2021MC045), the Key Research & Development Plan (Major Scientific and Technological Innovation Project) of Shandong Province, China (2021LZGC024) and the earmarked fund for China Agriculture Research System (CARS-27).

About author: XU Peng-yue, E-mail: x15610341272@163.com; #Correspondence LI Lin-guang, E-mail: lilinguang@shandong.cn; WANG Hai-bo, E-mali: wanghaibo992@126.com * These authors contributed equally to this study.

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XU Peng-yue, XU Li, XU Hai-feng, HE Xiao-wen, HE Ping, CHANG Yuan-sheng, WANG Sen, ZHENG Wen-yan, WANG Chuan-zeng, CHEN Xin, LI Lin-guang, WANG Hai-bo. 2023.

MdWRKY40is directly promotes anthocyanin accumulation and blocks MdMYB15L, the repressor of MdCBF2, which improves cold tolerance in apple . Journal of Integrative Agriculture, 22(6): 1704-1719.

Agarwal M, Hao Y J, Kapoor A, Dong C H, Fujii H, Zheng X, Zhu J K. 2006. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. Journal of Biological Chemistry, 281, 37636-37645.

Alessandra A, Erika C, Sara Z, Laura F, Maura B, Benedetto R, Battista T G. 2017. A grapevine TTG2-Like WRKY transcription factor is involved in regulating vacuolar transport and flavonoid biosynthesis. Frontiers in Plant Science, 7, 1979.

An J P, Wang X F, Zhang X W, You C X, Hao Y J. 2021. Apple B-box protein BBX37 regulates jasmonic acid mediated cold tolerance through the JAZ-BBX37-ICE1-CBF pathway and undergoes MIEL1-mediated ubiquitination and degradation. New Phytologist, 229, 2707-2729.

An J P, Zhang X W, You C X, B S Q, Wang X F, Hao Y J. 2019. MdWRKY40 promotes wounding-induced anthocyanin biosynthesis in association with MdMYB1 and undergoes MdBT2-mediated degradation. New Phytologist, 224, 380-395.

Angersbach A, Heinz V, Knorr D. 1999. Electrophysiological model of intact and processed plant tissues: cell disintegration criteria. Biotechnology Progress, 15, 753-762.

Brugière N, Dubois F, Limami A M, Lelandais M, Roux Y, Sangwan R S, Hirel B. 1999. Glutamine synthetase in the phloem plays a major role in controlling proline production. The Plant Cell, 11, 1995-2011.

Chagné D, Lin-Wang K, Espley R V, Volz R K, How N M, Rouse S, Brendolise C, Carlisle C M, Kumar S, Silva N D, Micheletti D, McGhie T, Crowhurst R N, Storey R D, Velasco R, Hellens R P, Gardiner S E, Allan A C. 2013. An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiology, 161, 225-239.

Chen L G, Song Y, Li S J, Zhang L P, Zou C S, Yu D Q. 2012. The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta, 1819, 120-128.

Chen T H, Murata N. 2002. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Current Opinion in Plant Biology, 5, 250-257.

Chi Y J, Yang Y, Zhou Y, Zhou J, Fan B F, Yu J Q, Chen Z X. 2013. Protein–protein interactions in the regulation of WRKY transcription factors. Molecular Plant, 6, 287-300.

Chinnusamy V, Zhu J, Zhu J K. 2007. Cold stress regulation of gene expression in plants. Trends in Plant Science, 12, 444-451.

Ciolkowski I, Wanke D, Birkenbihl R P, Somssich I E. 2008. Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Molecular Biology, 68, 81-92.

Cook D, Fowler S, Fiehn O, Thomashow M F. 2004. A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 101, 15243-15248.

Cui D L, Zhao S X, Xu H N, Allan A C, Zhang X D, Fan L, Chen L M, Su J, Shu Q, Li K Z. 2021. The interaction of MYB, bHLH and WD40 transcription factors in red pear (Pyrus pyrifolia) peel. Plant Molecular Biology, 106, 407-417.

Deng C, Ye H, Fan M, Pu T, Yan J. 2017. The rice transcription factors OsICE confer enhanced cold tolerance in transgenic Arabidopsis. Plant Signaling and Behavior, 12, 786-802.

Devaiah B N, Karthikeyan A S, Raghothama K G. 2007. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiology, 143, 1789-1801.

Ding Y, Shi Y, Yang S. 2019. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytologist, 222, 1690-1704.

Duan S, Wang J, Gao C, Jin C, Li D, Peng D, Du G, Li Y, Chen, M. 2018. Functional characterization of a heterologously expressed Brassica napus WRKY41-1 transcription factor in regulating anthocyanin biosynthesis in Arabidopsis thaliana. Plant Science, 268, 47-53.

Espley R V, Brendolise C, Chagné D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten H J, Gardiner S E, Hellens R P, Allan A C. 2009. Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. The Plant Cell, 21, 168-183.

Eulgem T, Rushton P J, Robatzek S, Somssich I E. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science, 5, 199-206.

Fang H C, Dong Y H, Yue X X, Hu J F, Jiang S H, Xu H F, Wang Y C, Su M Y, Zhang J, Zhang Z Y, Wang N, Chen X S. 2019. The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature. Plant Cell and Environment, 42, 2090-2104.

Farajzadeh M, Rahimi M, Kamalib G A, Mavrommatisc T. 2010. Modelling apple tree bud burst time and frost risk in Iran. Meteorological Applications, 17, 45-52.

Field T S, Lee D W, Holbrook N M. 2001. Why leaves turn red in autumn. the role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiology, 127, 566-574.

Gilmour S J, Fowler S G, Thomashow M F. 2004. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Molecular Biology, 54, 767-781.

Hu Y R, Jiang L Q, Wang F, Yu D Q. 2013. jasmonate regulates the inducer of cbf expression–C-repeat binding factor/dre binding factor1 cascade and freezing tolerance in Arabidopsis. The Plant Cell, 25, 2907-2924.

Jaakola L. 2013. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends in Plant Science, 18, 477-483.

Ji X H, Wang Y T, Zhang R, Wu S J, An M M, Li M, Wang C Z, Chen X L, Zhang Y M, Chen X S. 2015. Effect of auxin, cytokinin and nitrogen on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Cell Tissue Organ Cult, 120, 325-337.

Jia Y, Ding Y, Shi Y, Zhang X, Gong Z, Yang S. 2016. The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytologist, 212, 345-353.

Jiang B C, Shi Y T, Zhang X Y, Xin X Y, Qi L J, Guo H W, Li J G, Yang S H. 2017. PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 114, 6695-6702.

Kidokoro S, Yoneda K, Takasaki H, Takahashi F, Shinozaki K, Yamaguchi-Shinozaki K. 2017. Different cold-signaling pathways function in the responses to rapid and gradual decreases in temperature. The Plant Cell, 29, 760-774.

Kratsch H A, Wise R R. 2000. The ultrastructure of chilling stress. Plant Cell and Environment, 23, 337-350.

Kui L W, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie T K, Espley R V, Hellens R P, Allan A C. 2010. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biology, 10, 50.

Leng P, Qi J X. 2003. Effect of anthocyanin on David peach (Prunus davidiana Franch) under low temperature stress. Scientia Horticulturae, 97, 27-39.

Li C, Wu J, Hu K D, Wei S W, Sun H Y, Hu L Y, Han Z, Yao G F, Zhang H. 2020. PyWRKY26 and PybHLH3 cotargeted the PyMYB114 promoter to regulate anthocyanin biosynthesis and transport in red-skinned pears. Horticulture Research, 7, 37.

Li H, Ye K, Shi Y, Cheng J, Zhang X, Yang S. 2017. BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Molecular Plant, 10, 545-559.

Li Y M, Zhu L, Zhu H Y, Song P Y, Guo L Q, Yang L M. 2018. Genome-wide analysis of the WRKY family genes and their responses to cold stress in watermelon. Czech Journal of Genetics and Plant Breeding, 54, 168-176.

Liu W J, Wang Y C, Yu L, Jiang H Y, Guo Z W, Xu H F, Jiang S H, Fang H C, Zhang J, Su M Y, Zhang Z Y, Chen X L, Chen X S, Wang N. 2019. MdWRKY11 participates in anthocyanin accumulation in red-fleshed apples by affecting MYB transcription factors and the photoresponse factor MdHY5. Journal of Agricultural and Food Chemistry, 67, 8783-8793.

Luo D L, Ba L J, Shan W, Kuang J F, Lu W J, Chen J Y. 2017. Involvement of WRKY transcription factors in Abscisic-Acid-induced cold tolerance of banana fruit. Journal of Agricultural and Food Chemistry, 65, 3627-3635.

Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K. 2004. Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. The Plant Journal, 38, 982-993.

Mittler R, Vanderauwera S, Gollery M, Breusegem F V. 2004. Reactive oxygen gene network of plants. Trends in Plant Science, 9, 1360-1385.

Niu C F, Wei W, Zhou Q Y, Tian A G, Han Y J, Zhang W K, Ma B, Lin Q, Zhang Z B, Zhang J S, Chen S Y. 2012. Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell and Environment, 35, 1156-1170.

Nosenko T, Bondel K B, Kumpfmuller G, Stephan W. 2016. Adaptation to low temperatures in the wild tomato species Solanum chilense. Molecular Ecology, 25, 2853-2869.

Ohya T. 1993. Reactivity of alkanals towards malondialdehyde (MDA) and the effect of alkanals on MDA determination with a thiobarbituric acid test. Biological & Pharmaceutical Bulletin, 16, 1078-1082.

Qiu Z K, Wang H J, Li D J, Yu B W, Hui Q L, Yan S S, Huang Z J, Cui X, Cao B H. 2019. Identification of candidate HY5-dependent and-independent regulators of anthocyanin biosynthesis in tomato. Plant and Cell Physiology, 60, 643-656.

Ramamoorthy R, Jiang S Y, Kumar N, Venkatesh P N, Ramachandran S. 2008. A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant and Cell Physiology, 49, 865-879.

Ravaglia D, Espley R V, Henry-Kirk R A, Andreotti C, Ziosi V, Hellens R P, Costa G, Allan A C. 2013. Transcriptional regulation of flavonoid biosynthesis in nectarine (Prunus persica) by a set of R2R3 MYB transcription factors. BMC Plant Biology, 13, 68.

Robison J D, Yamasaki Y, Randall S K. 2019. The ethylene signaling pathway negatively impacts CBF/DREB-regulated cold response in soybean (Glycine max). Frontiers in Plant Science, 10, 121-138.

Ruelland E, Vaultier M N, Zachowski A, Hurry V. 2009. Cold signalling and cold acclimation in plants. Advances in Botanical Research, 49, 35-150.

Stitt M, Hurry V A. 2002. Plant for all seasons: Alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Current Opinion in Plant Biology, 5, 199-206.

Sun Q R, Sun H Y, Bell R L, Li L G, Xin L, Tao J H, Li Q. 2014. Optimisation of the media for in vitro shoot proliferation and root induction in three new cold-hardy and dwarfing or semi-dwarfing clonal apple rootstocks. Journal of Horticultural Science & Biotechnology, 89, 381-388.

Sun X M, Zhang L L, Wong D C J, Wang Y, Zhu Z F, Xu G Z, Wang Q F, Li S H, Liang Z C, Xin H P. 2019. The ethylene response factor VaERF092 from Amur grape regulates the transcription factor VaWRKY33, improving cold tolerance. The Plant Journal, 99, 988-1002.

Verweij W, Spelt C E, Bliek M, de Vries M, Wit N, Faraco M, Koes R, Quattrocchio F M. 2016. Functionally similar WRKY proteins regulate vacuolar acidification in petunia and hair development in Arabidopsis. The Plant Cell, 28, 786-803.

Wang F, Guo Z X, Li H Z, Wang M M, Onac E, Zhou J, Xia X J, Shi K, Yu J Q, Zhou Y H. 2016. Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiology, 170, 459-471.

Wang L N, Zhu W, Fang L C, Sun X M, Su L Y, Liang Z C, Wang N, Londo J P, Li S H, Xin H P. 2014. Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biology, 14, 103.

Wang M Q, Huang Q X, Lin P, Zeng Q H, Li Y, Liu Q L, Zhang L, Pan Y Z, Jiang B B, Zhang F. 2020. The Overexpression of a Transcription Factor Gene VbWRKY32 Enhances the Cold Tolerance in Verbena bonariensis. Frontiers in Plant Science, 10, 1746.

Wang N, Qu C Z, Jiang S H, Chen Z J, Xu H F, Fang H C, Su M Y, Zhang J, Wang Y C, Liu W J, Zhang Z Y, Lu N L, Chen X S. 2018. The proanthocyanidin-specific transcription factor MdMYBPA1 initiates anthocyanin synthesis under low-temperature conditions in red-fleshed apples. The Plant Journal, 96, 39-55.

Xi W P, Feng J, Liu Y, Zhang S K, Zhao G H. 2019. The R2R3-MYB transcription factor PaMYB10 is involved in anthocyanin biosynthesis in apricots and determines red blushed skin. BMC Plant Biology, 19, 287.

Xu H F, Yang G X, Zhang J, Wang Y C, Zhang T L, Wang N, Jiang S H, Zhang Z Y, Chen X S. 2018. Overexpression of a repressor MdMYB15L negatively regulates anthocyanin and cold tolerance in red-fleshed callus. Biochemical and Biophysical Research Communications, 500, 405-410.

Xu H F, Zou Q, Yang G X, Jiang S H, Fang H C, Wang Y C, Zhang J, Zhang Z Y, Wang N, Chen X S. 2020. MdMYB6 regulates anthocyanin formation in apple both through direct inhibition of the biosynthesis pathway and through substrate removal. Horticulture Research, 7, 72.

Xu W, Dubos C, Lepiniec L. 2015. Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends in Plant Science, 20, 176-185.

Ye Y J, Xiao Y Y, Han Y C, Shan W, Fan Z Q, Xu Q G, Kuang J F, Lu W J, Lakshmanan P, Chen J Y. 2016. Banana fruit VQ motif-containing protein5 represses cold-responsive transcription factor MaWRKY26 involved in the regulation of JA biosynthetic genes. Scientific Reports, 6, 18643-18655.

Zhang J, Xu H F, Wang N, Jiang S H, Fang H C, Zhang Z Y, Yang G X, Wang Y C, Su M Y, Xu L, Chen X S. 2018. The ethylene response factor MdERF1B regulates anthocyanin and proanthocyanidin biosynthesis in apple. Plant Molecular Biology, 98, 205-218.

Zhang M X, Zhao R R, Huang K, Huang S Z, Wang H T, Wei Z Q, Li Z, Bian M D, Jiang W Z, Wu T, Du X L. 2022. The OsWRKY63–OsWRKY76–OsDREB1B module regulates chilling tolerance in rice. The Plant Journal, 112, 383-398.

Zhang Y, Yu H J, Yang X Y, Li Q, Ling J, Wang H, Gu X F, Huang S W, Jiang W J. 2016. CsWRKY46, a WRKY transcription factor from cucumber, confers cold resistance in transgenic-plant by regulating a set of cold-stress responsive genes in an ABA-dependent manner. Plant Physiology and Biochemistry, 108, 478-487.

Zhang Y J, Wang L J. 2005. The WRKY transcription factor superfamily: Its origin in eukaryotes and expansion in plants. BMC Evolutionary Biology, 5, 1-12.

Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu J K. 2016. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiology, 171, 2744-2759.

Zhu J K. 2016. Abiotic stress signaling and responses in plants. Cell, 167, 313-324.

Zou C, Jiang W, Yu D. 2010. Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. Journal of Experimental Botany, 61, 3901-3914.

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