The trade-off between UVB sensitivity and tolerance against other stresses in African rice species

The trade-off between UVB sensitivity and tolerance against other stresses in African rice species

Climate change and ozone depletion have caused increased ultraviolet B (UVB; 280-315nm) radiation levels on earth, which has been predicted to cause decreased growth and yield of various crops, including rice, the most important staple food worldwide. UVB radiation sensitivity varies extensively in Asian rice (Oryza sativa L.) and African rice (Oryza glaberrima Steud. and Oryza barthii A. Chev.) cultivars, and the activity of cyclobutane pyrimidine dimer (CPD) photolyase that repairs UVB-induced CPD is an essential factor underlying UVB sensitivity in rice. Unlike Asian varieties, African rice possesses different origins, and it is cultivated in the African continent under environmental stresses and unstable climatic conditions and is well-adapted to various biotic and abiotic stresses. However, information regarding UVB sensitivity in African rice remains lacking. In this review, we describe recent research examining the sensitivity of rice species to UVB radiation, and we focus on UVB sensitivity and CPD photolyase genotypes with emphasis on African rice species. Consequently, the novel CPD photolyase genotype found only in African rice species results in a more severe phenotype termed “Super-hypersensitive” in cultivars grown only in West Africa, particularly at O. glaberrima domestication centres. We also describe possible reasons for the high UVB sensitivity of African rice cultivars in relation to plant morphology and other environmental stresses such as floods and pathogens. Finally, using the available knowledge, we suggest possible ways to develop multiple stress-resistant plants that can cope well in tropical environments under numerous environmental stresses. This review provides more tools for increasing food production for feeding the outgrowing population, particularly in tropical areas such as Africa.

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  • Agnoun Y, Biaou SSH, Sié M, Vodouhè RS, Ahanchédé A (2012). The African rice Oryza glaberrima Steud: Knowledge distribution and prospects. International Journal of Biology 4: 158-180. doi:10.5539/ijb.v4n3p158
  • Bandurska H, Cieślak M (2013). The interactive effect of water deficit and UV-B radiation on salicylic acid accumulation in barley roots and leaves. Environmental and Experimental Botany 94: 9-18. doi: 10.1016/j.envexpbot.2012.03.001
  • Brar DS, Khush GS (1997). Alien introgression in rice. Plant Molecular Biology 35: 35-47. doi: 10.1023/A:1005825519998
  • Brash DE, Seetharamt S, Kraemertt KH, Seidmant MM, Bredbergt A (1987). Photoproduct frequency is not the major determinant of UV base substitution hot spots or cold spots in human cells (UV carcinogenesis/DNA structure/xeroderma pigmentosum/DNA repair/shuttle vector). Proceedings of the National Academy of Sciences of United States of America 84: 3782-3786. doi: 10.1073/pnas.84.11.3782
  • Brash DE, Rudolph JA, Simon JA, Lin A, McKenna GJ et al. (1991). A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proceedings of the National Academy of Sciences of United States of America 88: 10124- 10128. doi: 10.1073/pnas.88.22.10124
  • Britt AB (1996). DNA damage and repair in plants. Annual Reviews of Plant Biology 47: 75-100. doi: 10.1146/annurev. arplant.47.1.75
  • Britt AB (1999). Molecular genetics of DNA repair in higher plants. Trends in Plant Science 4: 20-25. doi: 10.1016/S1360- 1385(98)01355-7
  • Britt AB, Chen JJ, Wykoff D, Mitchell D (1993). A UV-sensitive mutant of Arabidopsis defective in the repair of pyrimidinepyrimidinone(6-4) dimers. Science. 261: 1571-1574. doi: 10.1126/science.8372351
  • Brosché M, Strid Å (2003). Molecular events following perception of ultraviolet‐B radiation by plants. Physiologia Plantarum. 117: 1-10. doi: 10.1034/j.1399-3054.2003.1170101.x
  • Brown JKM (2002). Yield penalties of disease resistance in crops. Current Opinion Plant Biology 5: 339-344. doi: 10.1016/ S1369-5266(02)00270-4
  • Brown JKM, Rant JC (2013). Fitness costs and trade-offs of disease resistance and their consequences for breeding arable crops. Plant Pathology 62: 83-95. doi: 10.1111/ppa.12163
  • Caldwell CR (1993). Ultraviolet-induced photodegradation of cucumber (Cucumis sativus L.) microsomal and soluble protein tryptophanyl residues in vitro. Plant Physiology. 101: 947-953. doi: 10.1104/pp.101.3.947
  • Casadevall R, Rodriguez RE, Debernardi JM, Palatnik JF, Casati P (2013). Repression of growth regulating factors by the microRNA396 inhibits cell proliferation by UV-B radiation in Arabidopsis leaves. Plant Cell 25: 3570-3583. doi: 10.1105/ tpc.113.117473
  • Chalker‐Scott L, Scott JD (2004). Elevated ultraviolet‐B radiation induces cross‐protection to cold in leaves of Rhododendron under field conditions. Photochemical and Photobiology 79: 199-204. doi: 10.1562/0031-8655(2004)079<0199:eurict>2.0. co;2
  • Cockell CS, Horneck G (2001). The history of the UV Radiation climate of the earth—theoretical and space‐based observations. Photochemical and Photobiology 73: 447-451. doi: 10.1562/0031-8655(2001)073<0447:thotur>2.0.co;2.
  • Demkura PV, Ballaré CL (2012). UVR8 mediates UV-B-induced arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Molecular Plant 5: 642-652. doi: 10.1093/mp/sss025
  • Filkowski J, Kovalchuk O, Kovalchuk I (2004). Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. Plant Journal 38: 60-69. doi: 10.1093/mp/sss025
  • Fina J, Casadevall R, AbdElgawad H, Prinsen E, Markakis MN et al. (2017). UV-B inhibits leaf growth through changes in growth regulating factors and gibberellin levels. Plant Physiology 174: 1110-1126. doi: 10.1104/pp.17.00365
  • Foyer CH, Lelandais M, Kunert KJ (1994). Photooxidative stress in plants. Physiologia Plantarum 92: 696-717. doi: 10.1111/ j.1399-3054.1994.tb03042.x
  • Frohnmeyer H, Loyall L, Blatt MR, Grabov A (1999). Millisecond UV-B irradiation evokes prolonged elevation of cytosolicfree Ca2+ and stimulates gene expression in transgenic parsley cell cultures. Plant Journal. 20: 109-117. doi: 10.1046/j.1365- 313x.1999.00584.x
  • Fujibe T, Saji H, Arakawa K, Yabe N, Takeuchi Y et al. (2004). A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiology 134: 275-85. doi: 10.1104/pp.103.033480
  • Gitz DC, Liu‐Gitz L (2003). How do UV photomorphogenic responses confer water stress tolerance?. Photochemistry and Photobiology 78: 529-534. doi: 10.1562/0031-8655(2003)0780529HDUPRC2.0.CO2
  • Gupta DK, Palma JM, Corpas FJ (2015). In Gupta DK, Palma JM, Corpas FJ (editors) Reactive oxygen species and oxidative damage in plants under stress. Springer, Heidelberg, pp. 1-22. doi:10.1007/978-3-319-20421-5
  • Hidema J, Kang H, Kumagai T (1996). Differences in the sensitivity to UVB radiation of two cultivars of rice (Oryza sativa L .). Plant & Cell Physiology 37: 742-747. doi: 10.1093/oxfordjournals. pcp.a029008
  • Hidema J, Kumagai T, Sutherland JC, Sutherland BM (1997). Ultraviolet B-sensitive rice cultivar deficient in cyclobutyl pyrimidine dimer repair. Plant Physiology 113: 39-44. doi: 10.1104/pp.113.1.39
  • Hidema J, Kumagai T, Sutherland BM (2000). UV radiation-sensitive norin 1 rice contains defective cyclobutane pyrimidine dimer photolyase. Plant Cell 12: 1569-78. doi: 10.1105/tpc.12.9.1569
  • Hidema J, Song IK, Sato T, Kumagai T (2001). Relationship between ultraviolet-B sensitivity and cyclobutane pyrimidine dimer photorepair in rice. Journal of Radiation Research 42: 295-303. doi: 10.1269/jrr.42.295
  • Hidema J, Teranishi M, Iwamatsu Y, Hirouchi T, Ueda T et al. (2005). Spontaneously occurring mutations in the cyclobutane pyrimidine dimer photolyase gene cause different sensitivities to ultraviolet-B in rice. Plant Journal 43: 57-67. doi: 10.1111/j.1365-313X.2005.02428.x
  • Hidema J, Kumagai T (2006). Sensitivity of rice to ultraviolet-B radiation. Annals of Botany 97: 933-942. doi: 10.1093/aob/ mcl044
  • Hidema J, Taguchi T, Ono T, Teranishi M, Yamamoto K et al. (2007). Increase in CPD photolyase activity functions effectively to prevent growth inhibition caused by UVB radiation. Plant Journal 50: 70-79. doi: 10.1111/j.1365-313X.2007.03041.x
  • Hollosy F (2002). Evaluation of lipophilicity and antitumour activity of parallel carboxamide libraries. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences 780: 355-363. doi: 10.1016/s1570-0232(02)00545-7.
  • Hopkins L, Bond MA, Tobin AK (2002). Ultraviolet-B radiation reduces the rates of cell division and elongation in the primary leaf of wheat (Triticum aestivum L. cv Marls Huntsman). Plant, Cell & Environment 25: 617-624. doi: 10.1046/j.1365- 3040.2002.00834.x
  • Horneck G, Klaus DM, Mancinelli RL (2010). Space microbiology. Microbiology Molecular Biology Review 74: 121-156. doi: 10.1128/MMBR.00016-09
  • Iwamatsu Y, Aoki C, Takahashi M, Teranishi M, Ding Y et al. (2008). UVB sensitivity and cyclobutane pyrimidine dimer (CPD) photolyase genotypes in cultivated and wild rice species. Photochemical & Photobiology Sciences 7: 311-320. doi: 10.1039/B719034D
  • Jablonski NG, Chaplin G (2010). Human skin pigmentation as an adaptation to UV radiation. Proceedings of the National Academy of Sciences of United States of America 107: 8962- 8968. doi: 10.1073/pnas.0914628107
  • Jackson MB, Ram PC (2003). Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Annals of Botany 91: 227-241. doi: 10.1093/aob/ mcf242
  • Jansen MAK, Gaba V, Greenberg BM (1998). Higher plants and UV-B radiation: Balancing damage, repair and acclimation. Trends in Plant Science 3: 131-135. doi: 10.1016/S1360-1385(98)01215-1
  • Kalbin G, Hidema J, Brosché M, Kumagai T, Bornman JF et al. (2001). UV-B-induced DNA damage and expression of defence genes under UV-B stress: Tissue-specific molecular marker analysis in leaves. Plant, Cell & Environment 24: 983-990. doi: 10.1046/j.1365-3040.2001.00748.x
  • Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997). Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9: 627-640. doi: 10.1105/tpc.9.4.627.
  • Kende H, van der Knaap E, Cho H-T (2002). Deepwater Rice: A Model Plant to Study Stem Elongation. Plant Physiol. 118: 1105-1110.
  • Kobayashi M, Kanto T, Fujikawa T, Yamada M, Ishiwata M et al. (2014). Supplemental UV radiation controls rose powdery mildew disease under the greenhouse conditions. Environmental Control in Biology 51: 157-163. doi: 10.2525/ ecb.51.157
  • Kucera B, Leubner-Metzger G, Wellmann E (2003). Distinct ultraviolet-signaling pathways in bean leaves. DNA Damage is associated with β-1,3-glucanase gene induction, but not with flavonoid formation. Plant Physiology 133: 1445-1452. doi: 10.1104/pp.103.029520
  • Kumagai T, Hidema J, Kang HS, Sato T (2001). Effects of supplemental UV-B radiation on the growth and yield of two cultivars of Japanese lowland rice (Oryza sativa L.) under the field in a cool rice-growing region of Japan. Agriculture Ecosystems & Environment Ecosyst. Environ. 83: 201-208. doi: 10.1016/ S0167-8809(00)00180-8
  • Kunz BA, Cahill DM, Mohr PG, Osmond MJ, Vonarx EJ (2006). Plant responses to UV radiation and links to pathogen resistance. International Review of Cytology 255: 1-40. doi: 10.1016/ S0074-7696(06)55001-6
  • Kunz BA, Dando PK, Grice DM, Mohr PG, Schenk PM et al. (2008). UV-induced DNA damage romotes resistance to the biotrophic pathogen Hyaloperonospora parasitica in Arabidopsis. Plant Physiology 148: 1021-1031. doi: 10.1104/pp.108.125435
  • Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993). Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5: 171-179. doi: 10.1105/tpc.5.2.171
  • Mackerness SAH (1997). Ultraviolet-B effects on transcript levels for photosynthetic genes are not mediated through carbohydrate metabolism. Plant, Cell & Environment 20: 1431-1437. doi: 10.1046/j.1365-3040.1997.d01-39.x
  • Mackerness SAH, Surplus SL, Blake P, John CF, Buchanan-Wollaston V et al. (1999). Ultraviolet-B-induced stress and changes in gene expression in Arabidopsis thaliana: role of signalling pathways controlled by jasmonic acid, ethylene and reactive oxygen species. Plant, Cell & Environment 22: 1413-1423. doi: 10.1046/j.1365-3040.1999.00499.x
  • Mackerness SAH, John CF, Jordan B, Thomas B (2001). Early signaling components in ultraviolet-B responses: Distinct roles for different reactive oxygen species and nitric oxide. FEBS Letters 489: 237-242. doi: 10.1016/S0014-5793(01)02103-2
  • Mazza CA, Zavala J, Scopel AL, Ballaré CL (1999). Perception of solar UVB radiation by phytophagous insects: behavioral responses and ecosystem implications. Proceedings of the National Academy of Sciences of United States of America 96: 980–985.
  • Mewis I, Schreiner M, Nguyen CN, Krumbein A, Ulrichs C et al. (2012). UV-B irradiation changes specifically the secondary metabolite profile in broccoli sprouts: induced signaling overlaps with defense response to biotic stressors. Plant & Cell Physiology 53: 1546-1560. doi: 10.1093/pcp/pcs096
  • Meyer RS, Choi YJ, Sanches M, Plessis A, Flowers JM et al. (2016). Domestication history and geographical adaptation inferred from a SNP map of African rice. Nature Genetics 48: 1083- 1088. doi:10.1038/ng.3633
  • Mitchell DL, Nairn RS (1989). The biology of the (6–4) photoproduct. Photochemistry and Photobiology 49: 805-819. doi: 10.1111/ j.1751-1097.1989.tb05578.x
  • Mmbando GS, Teranishi M, Hidema J (2020). Very high sensitivity of African rice to artificial ultraviolet-B radiation caused by genotype and quantity of cyclobutane pyrimidine dimer photolyase. Scientific Reports10: 1-14. doi: https://doi. org/10.1038/s41598-020-59720-x
  • Ndjiondjop MN, Manneh B, Cissoko M, Drame NK, Kakai RG et al. (2010). Drought resistance in an interspecific backcross population of rice (Oryza spp.) derived from the cross WAB56- 104 (O. sativa)×CG14 (O. glaberrima). Plant Science 179: 364- 373. doi: 10.1016/j.plantsci.2010.06.006
  • Neale RE, Barnes PW, Robson TM, Neale PJ, Williamson CE et al. (2020) Environmental effects of stratospheric ozone depletion, UV radiation, and interactions with climate change: UNEP Environmental Effects Assessment Panel, Update 2020. Photochemical & Photobiological Sciences: 20: 1–67. https:// doi.org/10.1007/s43630-020-00001-x
  • Oladele SO, Adegbaju MS, Awodun MA (2016). Harnessing the potentials of African rice (Oryza glaberrima Steud.) in the quest for self-sufficient and increased yield in sub-saharan Africa. Journal of Global and Ecology 4: 157-167. Website: https://www.ikprress.org/index.php/JOGAE/article/view/778
  • Pajerowska-Mukhtar KM, Wang W, Tada Y, Oka N, Tucker CL et al. (2012). The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Current Biology 22: 103-112. doi: 10.1016/j.cub.2011.12.015.
  • Pang Q, Hays JB (1991). UV-B-inducible and temperature-sensitive photoreactivation of cyclobutane pyrimidine dimers in Arabidopsis thaliana. Plant Physiology 95: 536-543. doi: 10.1104/pp.95.2.536
  • Parada RY, Mon-nai W, Ueno M, Kihara J, Arase S (2015). Red-lightinduced resistance to brown spot disease caused by Bipolaris oryzae in rice. Journal of Phytopathology 163: 116-123. doi: 10.1111/jph.12288
  • Piofczyk T, Jeena G, Pecinka A (2015). Arabidopsis thaliana natural variation reveals connections between UV radiation stress and plant pathogen-like defense responses. Plant Physiology and Biochemistry 93: 34-43. doi: 10.1016/j.plaphy.2015.01.011.
  • Porteres R (1955). History of the first samples of Oryza glaberrima collected from Africa. Journal of Tropical Agriculture and Appled Biology 2: 535-537.
  • Portères R (1955). Historique sur les premiers échantillons d’Oryza glaberrima St. recueillis en Afrique. Journal d’agriculture traditionnelle et de botanique appliquée 2: 535-537. https:// www.persee.fr/doc/jatba_0021-7662_1955_num_2_10_2257
  • Portères R (1962). Berceaux agricoles primaires sur le continent africain. Journal of African History 3: 195-210. http://www. jstor.org/stable/179739.
  • Portères R, Harlan J (1976). In Harlan JR, de Wet JMJ, Stamlar ABL (editors) The origin of African plant domestication. ASA Review of eBooks 5: 120-123. doi: 10.2307/532430
  • Poulson ME, Boeger MRT, Donahue RA (2006). Response of photosynthesis to high light and drought for Arabidopsis thaliana grown under a UV-B enhanced light regime. Photosynthetic Research 90: 79-90. doi: 10.1007/s11120-006-9116-2
  • Qi J, Zhang M, Lu C, Hettenhausen C, Tan Q, Cao G et al. (2018). Ultraviolet-B enhances the resistance of multiple plant species to lepidopteran insect herbivory through the jasmonic acid pathway. Scientific Reports 8: 1-9. doi: 10.1038/s41598-017- 18600-7
  • Quaite FE, Sutherland JC, Sutherland BM (1994). Isolation of highmolecular-weight plant DNA for DNA damage quantitation: relative effects of solar 297 nm UVB and 365 nm radiation. Plant Molecular Biology 24: 475-483. doi: 10.1007/BF00024115
  • Rajendiran K, Ramanujam MP (2003). Alleviation of ultraviolet-B radiation-induced growth inhibition of green gram by triadimefon. Biologia Plantarum 46: 621-624. doi: 10.1023/a:1024840301092
  • Ren J, Dai W, Xuan Z, Yao Y, Korpelainen H et al. (2007). The effect of drought and enhanced UV-B radiation on the growth and physiological traits of two contrasting poplar species. Forest Ecology and Managment 239: 112-119. doi: 10.1016/j. foreco.2006.11.014
  • Robson TM, Hartikainen SM, Aphalo PJ (2015). How does solar ultraviolet-B radiation improve drought tolerance of silver birch (Betula pendula Roth.) seedlings? Plant, Cell & Environment 38: 953-967. doi: 10.1111/pce.12405
  • Rodenburg J, Saito K, Kakaï RG, Touré A, Mariko M et al. (2009). Weed competitiveness of the lowland rice varieties of NERICA in the southern Guinea Savanna. Field Crops Research 114: 411- 418. doi:10.1016/j.fcr.2009.09.014
  • Sakagami J-I, Joho Y, Ito O (2009). Contrasting physiological responses by cultivars of Oryza sativa and O. glaberrima to prolonged submergence. Annals. Botany 103: 171-180. doi: 10.1093/aob/ mcn201
  • Sakagami J-I, Kawano N (2011). Survival of submerged rice in a floodprone region of West Africa. Tropics 20: 55-66. doi: 10.3759/ tropics.20.55
  • Sakagami J-I (2012). Submergence tolerance of rice species, Oryza glaberrima Steudel. Applied Photosynthesis 17: 353-364. doi: 10.5772/26023
  • Sancar A (1994). Mechanisms of DNA excision repair. Science. 266: 1954-1956. doi: 10.1126/science.7801120
  • Sanchez PL, Wing RA, Brar DS (2013). The wild relative of rice: Genomes and Genomics. Genetics and genomics of rice Spronger, New York, pp. 9-25. doi: 10.1007/978-1-4614-7903- 1_2
  • Sato T, Kumagai T (1993). Cultivar differences in resistance to the inhibitory effects of near-UV radiation among Asian ecotype and Japanese lowland and upland cultivars of rice (Oryza sativa L.). Japanese Journal of Breeding 43: 61-68. doi: 10.1270/ jsbbs1951.43.61
  • Second G (1985). In Sharma AK, Sharma A (editors) A new insight into the genome differentiation in Oryza L. through isozymic studies. Advancees in Chromosome and Cell Genetics Oxford & IBH, New Delhi, pp. 45-78. https://agris.fao.org/agrissearch/search.do?recordID=US201301441111
  • Semon M, Nielsen R, Jones MP, McCouch SR (2005). The population structure of African cultivated rice (Oryza glaberrima Steud.): evidence for elevated levels of linkage disequilibrium caused by admixture with O. sativa and ecological adaptation. Genetics 169: 1639-1647. doi: 10.1534/genetics.104.033175.
  • Soto-Suárez M, Baldrich P, Weigel D, Rubio-Somoza I, San Segundo B (2017). The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens. Scientific Reports 7: 1-14. doi:10.1038/srep44898
  • Teklemariam T, Blake TJ (2003). Effects of UVB preconditioning on heat tolerance of cucumber (Cucumis sativus L.). Environmental and Experimental Botany 50: 169-182. doi: 10.1016/S0098-8472(03)00024-8
  • Teramura AH (1983). Effects of ultraviolet‐B radiation on the growth and yield of crop plants. Physiologia Plantrum 58: 415-427. doi: 10.1111/j.1399-3054.1983.tb04203.x
  • Teramura AH, Sullivan JH, Lydon J (1990). Effects of UV‐B radiation on soybean yield and seed quality: a 6‐year field study. Physiologia Plantrum 80: 5-11. doi. https://doi. org/10.1111/j.1399-3054.1990.tb04367.x
  • Teramura AH, Ziska LH, Sztein AE (1991). Changes in growth and photosynthetic capacity of rice with increased UV‐B radiation. Physiologia Plantrum 83: 373–380. doi: https://doi. org/10.1111/j.1399-3054.1991.tb00108.x
  • Teranishi M, Iwamatsu Y, Hidema J, Kumagai T (2004). Ultraviolet-B sensitivities in Japanese lowland rice cultivars: cyclobutane pyrimidine dimer photolyase activity and gene mutation. Plant & Cell Physiololgy 45: 1848-1856. doi: 10.1093/pcp/pch215
  • Teranishi M, Taguchi T, Ono T, Hidema J (2012). Augmentation of CPD photolyase activity in japonica and indica rice increases their UVB resistance but still leaves the difference in their sensitivities. Photochemistry & Photobiology Sciences 11: 812- 820. doi: 10.1039/c2pp05392f
  • Ueda T, Sato T, Hidema J, Hirouchi T, Yamamoto K et al. (2005). qUVR-10, a major quantitative trait locus for ultraviolet-B resistance in rice, encodes cyclobutane pyrimidine dimer photolyase. Genetics 171: 1941-1950. doi: 10.1534/ genetics.105.044735
  • Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T et al. (2001). Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO Journal 21: 6483-6493. doi: 10.1093/emboj/cdf646
  • Wang M, Yu Y, Haberer G, Marri PR, Fan C et al. (2014). The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nature Genetices 46: 982-988. doi: 10.1038/ng.3044
  • Nwanze KF, Terry ER (1996). West Africa Rice Development Association (WARDA) Annual Report 1996. https://pdf.usaid. gov/pdf_docs/Pnach999.pdf
  • Xu G, Yuan M, Ai C, Liu L, Zhuang E et al. (2017). uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 545: 491-494. doi: 10.1038/nature22372
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