miR398 regulation in rice of the responses to abiotic and biotic stresses depends on CSD1 and CSD2 expression
Yuzhu Lu A B , Zhen Feng B , Liying Bian B , Hong Xie A B and Jiansheng Liang A B C
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou 225009, China.
B College of Bioscience and Biotechnology, Yangzhou University, Yangzhou 225009, China.
C Corresponding author. Email: jsliang@yzu.edu.cn
Functional Plant Biology 38(1) 44-53 https://doi.org/10.1071/FP10178
Submitted: 25 August 2010 Accepted: 24 October 2010 Published: 17 December 2010
Abstract
MiR398 targets two Cu or Zn superoxide dismutases (CSD1 and CSD2) in Arabidopsis thaliana (L.) Heynh. Here we provide evidence that rice (Oryza sativa L.) miR398 mediates responses to abiotic and biotic stresses through regulating the expression of its target genes, Os-CSD1 and Os-CSD2. Rice plants were exposed to various stresses, including high Cu2+, high salinity, high light, methyl viologen, water stress, pathogens and ethylene, and the molecular response was investigated. Rice plants overexpressing Os-miR398 and the miR398-resistant form of Os-CSD2 were also exposed to these stresses. Both abiotic and biotic stresses significantly inhibited Os-miR398 expression and thus stimulated the expression of Os-CSD1 and Os-CSD2. The plant hormone ethylene produced an especially marked response. Transgenic rice lines that overexpressed Os-miR398 had a lower expression of CSD1 and -2 and were more sensitive to environmental stress. Conversely, transgenic rice lines which overexpressed the miR398-resistant form of Os-CSD2 showed more tolerance to high salinity and water stress than non-transgenic rice. We conclude that Os-miR398 regulates the responses of rice to a wide range of environmental stresses and to ethylene, and exerts its role through mediating CSDs expression and cellular ROS levels.
Additional keywords: reactive oxygen species, ROS, superoxide dismutases.
References
Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. The Journal of Biological Chemistry 283, 15 932–15 945.| MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFert7k%3D&md5=8d178511ddbc082c78db908989a70ae1CAS |
Ashraf M, Ali Q (2008) Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.). Environmental and Experimental Botany 63, 266–273.
| Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVejtbk%3D&md5=9b99d6bfac761f7a2ac484990ea28550CAS |
Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. The Plant Cell 17, 1658–1673.
| Antiquity of microRNAs and their targets in land plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsVygu7o%3D&md5=fb80b47ed4a86a1261c894f797dedd20CAS | 15849273PubMed |
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. CRC Critical Reviews in Plant Sciences 24, 23–58.
| Drought and salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis12ns7c%3D&md5=97923046de4ec3106e9db9c162591817CAS |
Beauclair L, Yu A, Bouché N (2010) MicroRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. The Plant Journal 62, 454–462.
| MicroRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFygsLo%3D&md5=b3988073aeccaab95c8a6d597ace5732CAS | 20128885PubMed |
Bonnet E, Wuyts J, Rouze P, de Peer YV (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proceedings of the National Academy of Sciences of the United States of America 101, 11 511–11 516.
| Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVKgu7g%3D&md5=dc6dffc4e8b46e6284d57844fc05b1a4CAS |
Coupe SA, Palmer BG, Lake JA, Overy SA, Oxborough K, Woodward FI, Gray JE, Quick WP (2006) Systemic signalling of environmental cues in Arabidopsis leaves. Journal of Experimental Botany 57, 329–341.
| Systemic signalling of environmental cues in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKnsA%3D%3D&md5=817837d34316ce6e61d9aacc7bd67a5fCAS | 16330523PubMed |
Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Molecular Biology 67, 403–417.
| Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmslOmur8%3D&md5=f5a3371d651adb2b0973dbfe3fdb5ca0CAS | 18392778PubMed |
Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum 119, 355–364.
| Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslekt74%3D&md5=0c05429fa3f2d24deea8b6b4e00f5e07CAS |
Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056–1071.
| Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSgs70%3D&md5=10f289a34c66d22a30cedd84895e78ffCAS |
Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant, Cell & Environment 17, 507–523.
| Protection against oxygen radicals: an important defense mechanism studied in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXkslGgurg%3D&md5=08e6fb5a686957cbec4e3c3f23307574CAS |
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology 9, 436–442.
| Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks.Crossref | GoogleScholarGoogle Scholar | 16759898PubMed |
Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229, 1009–1014.
| Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1agsLY%3D&md5=3edaf870f041789ef69c9e60a7a53641CAS | 19148671PubMed |
Jia X, Wang WX, Ren L, Chen QJ, Mendu V, Willcut B, Dinkins R, Tang X, Tang G (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Molecular Biology 71, 51–59.
| Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVGjtbY%3D&md5=80365c3b91953ddce45c947ab89e7f45CAS | 19533381PubMed |
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant micro-RNAs and their targets, including a stress-induced miRNA. Molecular Cell 14, 787–799.
| Computational identification of plant micro-RNAs and their targets, including a stress-induced miRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlslemtrs%3D&md5=9b5a19cedfba567797059c05e69a9101CAS | 15200956PubMed |
Kim FJ, Kim HP, Hah YC, Roe JH (1996) Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. European Journal of Biochemistry 241, 178–185.
| Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1Cqtbs%3D&md5=e9a573de8ac9abf28546ecd90c57c085CAS | 8898904PubMed |
Kliebenstein DJ, Monde R, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology 118, 637–650.
| Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmslyqtb0%3D&md5=d25c4dcff4fb970f5cc75c40353c5f0bCAS | 9765550PubMed |
Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R (2010) Transcriptome-wide identification of microRNA targets in rice. The Plant Journal 62, 742–759.
| Transcriptome-wide identification of microRNA targets in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslCgsrw%3D&md5=d32fdd85d25385762abdc26d5b13fc52CAS | 20202174PubMed |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVWnu7Y%3D&md5=c064ba536e130cc3e7e051ddbf1db43eCAS | 12234732PubMed |
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.
| Reactive oxygen gene network of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotF2msrg%3D&md5=64ec0783e7038e311275ec58b1e042fdCAS | 15465684PubMed |
Patterson BD, Mackae EA, Fergusen IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Analytical Biochemistry 139, 487–492.
| Estimation of hydrogen peroxide in plant extracts using titanium (IV).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1SjtLs%3D&md5=4712cc73bdbeaeaf9de4cbf9397f6892CAS | 6476384PubMed |
Perl-Treves R, Galun E (1991) The tomato Cu, Zn superoxide dismutase genes are developmentally regulated and respond to light and stress. Plant Molecular Biology 17, 745–760.
| The tomato Cu, Zn superoxide dismutase genes are developmentally regulated and respond to light and stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslags7w%3D&md5=cc166b0b1bbcdd8bee2d63e0f2315e21CAS | 1912497PubMed |
Rizhsky L, Liang H, Mittler R (2003) The water–water cycle is essential for chloroplast protection in the absence of stress. The Journal of Biological Chemistry 278, 38 921–38 925.
| The water–water cycle is essential for chloroplast protection in the absence of stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnslWjtr8%3D&md5=c26071da284173123057510d7efd3802CAS |
Scandalios JG (1993) Oxygen stress and superoxide dismutases. Plant Physiology 101, 7–12.
Sharma YK, Davis KR (1997) The effects of ozone on antioxidant responses in plants. Free Radical Biology & Medicine 23, 480–488.
| The effects of ozone on antioxidant responses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVahur4%3D&md5=55464f1b6f02839fa92742f3c11de5bfCAS | 9214586PubMed |
Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends in Plant Science 14, 43–50.
| The relationship between metal toxicity and cellular redox imbalance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntVygsg%3D%3D&md5=40df49f53cc280cf5c8657b0181feae2CAS | 19070530PubMed |
Smirnoff N (1993) The role of active oxygen in the response of plants to water defcit and desiccation. New Phytologist 125, 27–58.
| The role of active oxygen in the response of plants to water defcit and desiccation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFams70%3D&md5=de77baf52c0c1796e35c50491896b9cfCAS |
Sunkar R, Zhu JK (2004) Novel and stress-regulated micro- RNAs and other small RNAs from Arabidopsis. The Plant Cell 16, 2001–2019.
| Novel and stress-regulated micro- RNAs and other small RNAs from Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVansb0%3D&md5=445feb88a19fcb159f059a3d1d2ed9ecCAS | 15258262PubMed |
Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. The Plant Cell 17, 1397–1411.
| Cloning and characterization of microRNAs from rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKksrc%3D&md5=8372fd74608e002cc97ce54e1bcc787fCAS | 15805478PubMed |
Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell 18, 2051–2065.
| Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xos1KjtLY%3D&md5=7bcd3c7cfc1a828849fc019fb2e88b7aCAS | 16861386PubMed |
Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiologia Plantarum 126, 45–51.
| Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKjtbg%3D&md5=9ab7a0e8183102478918229a9ab67954CAS |
Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes & Development 17, 49–63.
| A biochemical framework for RNA silencing in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlKrug%3D%3D&md5=88a5f897aee7b165071e4af3f57bd092CAS | 12514099PubMed |
Tsang EWT, Bowler C, Herouart D, Van Camp W, Villarroel R, Genetello C, Van Montagu M, Inze D (1991) Differential regulation of superoxide dismutases in plants exposed to environmental stress. The Plant Cell 3, 783–792.
Tuteja N, Sopory SK (2008) Plant signaling in stress: G-protein coupled receptors, heterotrimeric G-proteins and signal coupling via phospholipases. Plant Signaling & Behavior 3, 79–86.
| Plant signaling in stress: G-protein coupled receptors, heterotrimeric G-proteins and signal coupling via phospholipases.Crossref | GoogleScholarGoogle Scholar | 19516978PubMed |
van Loon LC, Geraats BP, Linthorst HJ (2006) Ethylene as a modulator of disease resistance in plants. Trends in Plant Science 11, 184–191.
| Ethylene as a modulator of disease resistance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVGnsLs%3D&md5=f7ae466381b9e3c421f3c5b2ac2734a1CAS | 16531096PubMed |
Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. The Biochemical Journal 322, 681–692.
Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. The Journal of Biological Chemistry 282, 16369–16378.
| Regulation of copper homeostasis by micro-RNA in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVajt7c%3D&md5=d312aabd548e21b350eb1c24d3755bf3CAS | 17405879PubMed |
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
| Salt and drought stress signal transduction in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhtbc%3D&md5=e4809e50947f06e8da6b900d2b2ac389CAS | 12221975PubMed |
