Levels of Crotonaldehyde and 4-hydroxy-(E)-2-nonenal and Expression of Genes Encoding Carbonyl-Scavenging Enzyme at Critical Node During Rice Seed Aging

doi:10.1016/j.rsci.2018.04.003

Abstract

Abstract:

The critical node (CN) is an important stage during seed aging, which is related to effective genebank conservation. Previous studies have demonstrated that proteins undergo carbonylated modification at the CN in rice, indicating oxidative damage. However, the levels of reactive carbonyl species (RCS) and the associated scavenging system at the CN are largely unknown. In this study, we optimized methods for the extraction and analysis of RCS from dry rice embryos. In order to acquire seeds at the CN, rice seeds were subjected to natural conditions for 7, 9, 11 and 13 months, and the seed germination rates were reduced to 90%, 82%, 71% and 57%, respectively. We chose the stage with seed germination rate of 82% as the CN according to the rice seed vigor loss curve. The levels of crotonaldehyde and 4-hydroxy-(E)-2-nonenal (HNE) were significantly increased at the CN. In addition, genes encoding carbonyl-scavenging enzyme, including OsALDHs and OsAKRs, were significantly down-regulated at the CN, and reductions in the expression of OsALDH2-2, OsALDH2-5, OsALDH3-4, OsALDH7, OsAKR1 and OsAKR2 in particular could be responsible for RCS accumulation. Thus, the accumulations of crotonaldehyde and HNE and down-regulation of genes encoding carbonyl-scavenging enzyme might be related to an accelerating loss of seed viability at the CN.

Key words: carbonyl-scavenging system, reactive carbonyl species, seed aging, crotonaldehyde, critical node, rice storage

Shenzao Fu, Guangkun Yin, Xia Xin, Shuhua Wu, Xinghua Wei, Xinxiong Lu. Levels of Crotonaldehyde and 4-hydroxy-(E)-2-nonenal and Expression of Genes Encoding Carbonyl-Scavenging Enzyme at Critical Node During Rice Seed Aging[J]. Rice Science, 2018, 25(3): 152-1604.

Figures/Tables 2

References 42

[1]	Alméras E, Stolz S, Vollenweider S, Reymond P, Mène-Saffrané L, Farmer E E.2003. Reactive electrophile species activate defense gene expression inArabidopsis. Plant J, 34(2): 205-216.
[2]	Csallany A S, Han I, Shoeman D W, Chen C, Yuan J Y.2015. 4-hydroxynonenal (HNE), a toxic aldehyde in French fries from fast food restaurants.J Am Oil Chem Soc, 92(10): 1413-1419.
[3]	FAO.2010. Second report on the state of the world’s plants genetic resources for food and agriculture. Commission on Genetic Resources for Food and Agriculture. Rome: Food and Agriculture Organization of the United Nations: 47.
[4]	Farmer E E, Mueller M J.2013. ROS-mediated lipid peroxidation and RES-activated signaling.Annu Rev Plant Biol, 64(1): 429-450.
[5]	Gao C X, Han B.2009. Evolutionary and expression study of the aldehyde dehydrogenase (ALDH) gene superfamily in rice (Oryza sativa). Gene, 431(1/2): 86-94.
[6]	Gao H Y, Jing L Q, Chen L, Ju J, Wang Y X, Zhu J G, Yang L X, Wang Y L.2016. Effects of elevated atmospheric CO2 and temperature on seed vigor of rice under open-air field conditions.Chin J Rice Sci, 30(4): 371-379. (in Chinese with English abstract)
[7]	Hay F R, de Guzman F, Ellis D, Makahiya H, Borromeo T, Hamilton N R S.2013. Viability of Oryza sativa L. seeds stored under genebank conditions for up to 30 years. Genet Resour Crop Evol, 60(1): 275-296.
[8]	Hay F R, de Guzman F, Hamilton N R S.2015. Viability monitoring intervals for genebank samples ofOryza sativa. Seed Sci Technol, 43(2): 218-237.
[9]	Hideg É, Nagy T, Oberschall A, Dudits D, Vass I.2003. Detoxification function of aldose/aldehyde reductase during drought and ultraviolet-B (280-320 nm) stresses.Plant Cell Environ, 26(4): 513-522.
[10]	Islam M M, Ye W, Matsushima D, Munemasa S, Okuma E, Nakamura Y, Biswas S, Mano J, Murata Y.2016. Reactive carbonyl species mediate ABA signaling in guard cells.Plant Cell Physiol, 57(12): 2552-2563.
[11]	ISTA.2014. International Rules for Seed Testing. Bassersdorf, Switzerland: International Seed Testing Association.
[12]	Kotchoni S O, Kuhns C, Ditzer A, Kirch H H, Bartels D.2006. Overexpression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ, 29(6): 1033-1048.
[13]	Lu X X, Chen X L, Guo Y H.2005. Seed germinability of 23 crop species after a decade of storage in the national genebank of China.Agric Sci China, 4(6): 408-412.
[14]	Mano J, Miyatake F, Hiraoka E, Tamoi M.2009. Evaluation of the toxicity of stress-related aldehydes to photosynthesis in chloroplasts.Planta, 230(4): 639-648.
[15]	Mano J.2012. Reactive carbonyl species: Their production from lipid peroxides, action in environmental stress, and the detoxification mechanism.Plant Physiol Biochem, 59: 90-97.
[16]	Mano J, Nagata M, Okamura S, Shiraya T, Mitsui T.2014. Identification of oxidatively modified proteins in salt-stressed Arabidopsis: A carbonyl-targeted proteomics approach. Plant Cell Physiol, 55(7): 1233-1244.
[17]	Matsui K, Sugimoto K, Kakumyan P, Khorobrykh S A, Mano J.2009. Volatile oxylipins and related compounds formed under stress in plants.Methods Mol Biol, 580: 17-28.
[18]	Matsui K, Sugimoto K, Mano J, Ozawa R, Takabayashi J.2012. Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements.PLoS One, 7(4): e36433.
[19]	Mène-Saffrané L, Davoine C, Stolz S, Majcherczyk P, Farmer E E.2007. Genetic removal of tri-unsaturated fatty acids suppresses developmental and molecular phenotypes of an Arabidopsis tocopherol-deficient mutant: Whole-body mapping of malondialdehyde pools in a complex eukaryote. J Biol Chem, 282: 35749-35756.
[20]	Mueller M J.1998. Radically novel prostaglandins in animals and plants: The isoprostanes.Chem Biol, 5(12): 323-333.
[21]	Nakazono M, Tsuji H, Li Y, Saisho D, Arimura S, Tsutsumi N, Hirai A.2000. Expression of a gene encoding mitochondrial aldehyde dehydrogenase in rice increases under submerged conditions.Plant Physiol, 124(2): 587-598.
[22]	Oberschall A, Deák M, Török K, Sass L, Vass I, Kovács I, Fehér A, Dudits D, Horváth G V.2000. A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses.Plant J, 24(4): 437-446.
[23]	Penning T M.2015. The aldo-keto reductases (AKRs): Overview.Chem-Biol Inter, 234(5): 236-246.
[24]	Rodrigues S M, Andrade M O, Gomes A P S, Damatta F M, Baracat-Pereira M C, Fontes E P B.2006. Arabidopsis and tobacco plants ectopically expressing the soybean antiquitin-like ALDH7 gene display enhanced tolerance to drought, salinity, and oxidative stress. J Exp Bot, 57(9): 1909-1918.
[25]	Sengupta D, Naik D, Reddy A R.2015. Plant aldo-keto reductases (AKRs) as multi-tasking soldiers involved in diverse plant metabolic processes and stress defense: A structure-function update.J Plant Physiol, 179: 40-55.
[26]	Shin J H, Kim S R, An G.2009. Rice aldehyde dehydrogenase 7 is needed for seed maturation and viability.Plant Physiol, 149(2): 905-915.
[27]	Stiti N, Adewale I O, Petersen J, Bartels D, Kirch H H.2011. Engineering the nucleotide coenzyme specificity and sulfhydryl redox sensitivity of two stress-responsive aldehyde dehydrogenase isoenzymes of Arabidopsis thaliana. Biochem J, 434(3): 459-471.
[28]	Sun Y L, Liu H M, Xu Q G.2017. Effects of cadmium stress on rice seed germination characteristics.Chin J Rice Sci, 31(4): 425-431. (in Chinese with English abstract)
[29]	Sunkar R, Bartels D, Kirch H H.2003. Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J, 35(4): 452-464.
[30]	Taylor N L, Day D A, Millar A H.2002. Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase.J Biol Chem, 277(45): 42663-42668.
[31]	Tsuji H, Meguro N, Suzuki Y, Tsutsumi N, Hirai A, Nakazono M.2003. Induction of mitochondrial aldehyde dehydrogenase by submergence facilitates oxidation of acetaldehyde during re-aeration in rice.Febs Lett, 546: 369-373.
[32]	Turóczy Z, Kis P, Török K, Cserháti M, Lendvai Á, Dudits D, Horváth G V.2011. Overproduction of a rice aldo-keto reductase increases oxidative and heat stress tolerance by malondialdehyde and methylglyoxal detoxification.Plant Mol Biol, 75(4/5): 399-412.
[33]	Vemanna R S, Vennapusa A R, Easwaran M, Chandrashekar B K, Rao H, Ghanti K, Sudhakar C, Mysore K S, Makarla U.2016. Aldo-keto reductase enzymes detoxify glyphosate and improve herbicide resistance in plants.Plant Biotechnol J, 15(7): 794-804.
[34]	Vemanna R S, Babitha K C, Solanki J K, Amarnatha Reddy V, Sarangi S K, Udayakumar M.2017. Aldo-keto reductase-1 (AKR1) protect cellular enzymes from salt stress by detoxifying reactive cytotoxic compounds.Plant Physiol Biochem, 113: 177-186.
[35]	Wang H, Jiang Z Z, Du H B, Liang C Y, Wang Y C, Zhang M H, Zhang L Y, Ye W C, Li P.2012. Simultaneous determination of three flavonoid C-glycosides in mice biosamples by HPLC- ESI-MS method after oral administration of Abrus mollis extract and its application to biodistribution studies. J Chromatogr B, 903: 68-74.
[36]	Weber H, Chételat A, Reymond P, Farmer E E.2004. Selective and powerful stress gene expression inArabidopsis in response to malondialdehyde. Plant J, 37(6): 877-888.
[37]	Xin X, Lin X H, Zhou Y C, Chen X L, Liu X, Lu X X.2011. Proteome analysis of maize seeds: The effect of artificial ageing.Physiol Planta, 143(2): 126-138.
[38]	Yamauchi Y, Hasegawa A, Taninaka A, Mizutani M, Sugimoto Y.2011. NADPH-dependent reductases involved in the detoxification of reactive carbonyls in plants.J Biol Chem, 286(9): 6999-7009.
[39]	Yin G K, Whelan J, Wu S H, Zhou J, Chen X L, Chen B Y, Zhang J M, Xin X, Lu X X.2016. Comprehensive mitochondrial metabolic shift during the critical node of seed ageing in rice.PLoS One, 11(4): e0148013.
[40]	Yin G K, Xin X, Fu S Z, An M N, Wu S H, Chen X L, Zhang J M, He J J, Whelan J, Lu X X.2017. Proteomic and carbonylation profile analysis at the critical node of seed ageing inOryza sativa. Sci Rep-UK, 7: 40611.
[41]	Yin L, Mano J, Wang S, Tsuji W, Tanaka K.2010. The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots.Plant Physiol, 152(3): 1406-1417.
[42]	Zhou J L, Wang X F, Jiao Y L, Qin Y H, Liu X G, He K, Chen C, Ma L G, Wang J, Xiong L Z, Zhang Q F, Fan L M, Deng X W.2007. Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle.Plant Mol Biol, 63(5): 591-608.

Gene	Accession	Gene description	Forward primer (5′-3′)	Reverse primer (5′-3′)	Production size (bp)
OsALDH2-1	AK119571	Aldehyde dehydrogenase 2-1	CCTCAGATTGACAAGGAGCA	GGCTCGATGTAGTACCCGTT	122
OsALDH2-2	AK101427	Aldehyde dehydrogenase 2-2	GGTCCTCAGGTTGACAAGGT	CTTTGTCACCAGTGGGTTTG	109
OsALDH2-3	CU607043	Aldehyde dehydrogenase 2-3	CAGGTGGACAAGGCTCAGTA	AATGGTGGGCTCGATGTAGT	126
OsALDH2-4	AK121610	Aldehyde dehydrogenase 2-4	TCTTGCCTGGATCACTTCAC	CATTGATGAGGAGCTTGGTG	120
OsALDH2-5	AK073079	Aldehyde dehydrogenase 2-5	AAGTCGTCCTTGAGTTGGCT	CATGGTCAACATCAGCATCA	105
OsALDH3-1	AK070741	Aldehyde dehydrogenase 3-1	ATAATCGGAGCGAAATGGTC	CAATCAGGAATGGTGCAAAC	94
OsALDH3-2	AK120274	Aldehyde dehydrogenase 3-2	AGGGTGGCAGCTTCTGTAGT	TTACCGTGATGATTGGGAGA	145
OsALDH3-3	AK071169	Aldehyde dehydrogenase 3-3	ATAGAGGACAGCATCGCCTT	ACTGCGTCGTTGAACGTAAC	134
OsALDH3-4	AK104746	Aldehyde dehydrogenase 3-4	ATTCCCATCAACTGCACAAA	TATGACTGGGTCGATGGAGA	100
OsALDH3-5	JC625236	Aldehyde dehydrogenase 3-5	GCTGCGATCATCTGACTTGT	TCGTCCATCAGCTTCTTCAG	72
OsALDH7	AK120185	Aldehyde dehydrogenase 7	AGAGCAAAGCTCCATCACCT	TGAACCTCTCCAATCCCTTC	80
OsAKR1	AK242899	Aldo-keto reductase 1	TCGATTGCATCGACCTTTAC	ATGCCGATGCTTCACATAAG	132
OsAKR2	AK103729	Aldo-keto reductase 2	CATCAGGGAAGCGATGTATG	CCTCGAACATCATCTGTGCT	143
OsAKR3	AK100718	Aldo-keto reductase 3	AGCTCACACCTGACGAGATG	GCGGAGGAGTTTCAGAGTTC	117
UBQ5	AK062354	Ubiquitin 5	ACCACTTCGACCGCCACTACT	ACGCC TAAGCCTGCTGGTT	69

Gene	Accession	Gene description	Forward primer (5′-3′)	Reverse primer (5′-3′)	Production size (bp)
OsALDH2-1	AK119571	Aldehyde dehydrogenase 2-1	CCTCAGATTGACAAGGAGCA	GGCTCGATGTAGTACCCGTT	122
OsALDH2-2	AK101427	Aldehyde dehydrogenase 2-2	GGTCCTCAGGTTGACAAGGT	CTTTGTCACCAGTGGGTTTG	109
OsALDH2-3	CU607043	Aldehyde dehydrogenase 2-3	CAGGTGGACAAGGCTCAGTA	AATGGTGGGCTCGATGTAGT	126
OsALDH2-4	AK121610	Aldehyde dehydrogenase 2-4	TCTTGCCTGGATCACTTCAC	CATTGATGAGGAGCTTGGTG	120
OsALDH2-5	AK073079	Aldehyde dehydrogenase 2-5	AAGTCGTCCTTGAGTTGGCT	CATGGTCAACATCAGCATCA	105
OsALDH3-1	AK070741	Aldehyde dehydrogenase 3-1	ATAATCGGAGCGAAATGGTC	CAATCAGGAATGGTGCAAAC	94
OsALDH3-2	AK120274	Aldehyde dehydrogenase 3-2	AGGGTGGCAGCTTCTGTAGT	TTACCGTGATGATTGGGAGA	145
OsALDH3-3	AK071169	Aldehyde dehydrogenase 3-3	ATAGAGGACAGCATCGCCTT	ACTGCGTCGTTGAACGTAAC	134
OsALDH3-4	AK104746	Aldehyde dehydrogenase 3-4	ATTCCCATCAACTGCACAAA	TATGACTGGGTCGATGGAGA	100
OsALDH3-5	JC625236	Aldehyde dehydrogenase 3-5	GCTGCGATCATCTGACTTGT	TCGTCCATCAGCTTCTTCAG	72
OsALDH7	AK120185	Aldehyde dehydrogenase 7	AGAGCAAAGCTCCATCACCT	TGAACCTCTCCAATCCCTTC	80
OsAKR1	AK242899	Aldo-keto reductase 1	TCGATTGCATCGACCTTTAC	ATGCCGATGCTTCACATAAG	132
OsAKR2	AK103729	Aldo-keto reductase 2	CATCAGGGAAGCGATGTATG	CCTCGAACATCATCTGTGCT	143
OsAKR3	AK100718	Aldo-keto reductase 3	AGCTCACACCTGACGAGATG	GCGGAGGAGTTTCAGAGTTC	117
UBQ5	AK062354	Ubiquitin 5	ACCACTTCGACCGCCACTACT	ACGCC TAAGCCTGCTGGTT	69