A novel gene, CaATHB-12, negatively regulates fruit carotenoid content under cold stress in Capsicum annuum

  • Rui-Xing Zhang College of Horticulture, Northwest A&F University, Yangling, Shaanxi, China
  • Wen-Chao Zhu Guizhou Institute of Pepper, Guiyang, China
  • Guo-Xin Cheng College of Horticulture, Northwest A&F University, Yangling, Shaanxi, China
  • Ya-Nan Yu College of Horticulture, Northwest A&F University, Yangling, Shaanxi, China
  • Quan-Hui Li College of Horticulture, Northwest A&F University, Yangling, Shaanxi, China
  • Saeed ul Haq College of Horticulture, Northwest A&F University, Yangling, Shaanxi, China
  • Fazal Said Department of Agriculture, Abdul Wali Khan University, Mardan, Paksitan
  • Zhen-Hui Gong College of Horticulture, Northwest A&F University, Yangling, Shaanxi, China
Keywords: pepper; Carotenoids; CaATHB-12; Cold stress; Transgenic Arabidopsis

Abstract

Background: Carotenoids, the secondary metabolites terpenoids, are the largest factors that form the fruit color. Similar to flavonoids, they are not only safe and natural colorants of fruits but also play a role as stress response biomolecules.

Methods: To study the contribution of the key genes in carotenoids biosynthesis, fruit-color formation, and in response to cold stress, we characterized the key regulatory factor CaATHB-12 from the HD-ZIP I sub-gene family members in pepper.

Results: Cold stress enhanced carotenoid accumulation as compared with the normal condition. CaATHB-12 silencing through virus-induced gene silencing changed the fruit color by regulating the carotenoid contents. CaATHB-12 silencing increased the antioxidant enzyme activities in the fruits of pepper, exposed to cold stress, whereas CaATHB-12 overexpression decreased the activities of antioxidant enzymes in the transgenic Arabidopsis lines, exposed to cold stress, suggesting that CaATHB-12 is involved in the regulation of cold stress in the pepper fruits.

Conclusion: Our research will provide insights into the formation of fruit color in pepper and contribution of CaATHB-12 in response to cold stress. Further study should be focused on the interaction between CaATHB-12 and its target gene.

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References


  1. León-Chan RG, López-Meyer M, Osuna-Enciso T, Sañudo-​Barajas JA, Heredia JB, León-Félix J. Low temperature and ultraviolet-B radiation affect chlorophyll content and induce the accumulation of UV-B-absorbing and antioxidant compounds in bell pepper (Capsicum annuum) plants. Environ Exp Bot 2017; 139: 143–51. doi: 10.1016/j.envexpbot.2017.05.006

  2. Kaniuga Z. Chilling response of plants: importance of galactolipase, free fatty acids and free radicals. Plant Biol 2010; 10(2): 171–84. doi: 10.1111/j.1438-8677.2007.00019.x

  3. Korkmaz A, Korkmaz Y, Demirkıran AR. Enhancing chilling stress tolerance of pepper seedlings by exogenous application of 5-aminolevulinic acid. Environ Exp Bot 2010; 67(3): 495–501. doi: 10.1016/j.envexpbot.2009.07.009

  4. Zhang W, Jiang B, Li W, Song H, Yu Y, Chen J. Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Sci Horticult 2009; 122(2): 200–8. doi: 10.1016/j.scienta.2009.05.013

  5. Guo W-L, Chen R-G, Gong Z-H, Yin Y-X, Li D-W. Suppression subtractive hybridization analysis of genes regulated by application of exogenous abscisic acid in pepper plant (Capsicum annuum L.) leaves under chilling stress. PLoS One 2013; 8(6). doi: 10.1371/journal.pone.0066667

  6. Mukherjee K, Brocchieri L, Bürglin TR. A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 2009; 26(12): 2775–94. doi: 10.1093/molbev/msp201

  7. Zhong Yf, Holland PW. HomeoDB2: functional expansion of a comparative homeobox gene database for evolutionary developmental biology. Evol Dev 2011; 13(6): 567–8. doi: 10.1111/j.1525-142x.2011.00513.x

  8. Holland PW. Evolution of homeobox genes. Wiley Interdisc Rev Dev Biol 2013; 2(1): 31–45. doi: 10.1002/wdev.78

  9. Ariel FD, Manavella PA, Dezar CA, Chan RL. The true story of the HD-Zip family. Trends Plant Sci 2007; 12(9): 419–26. doi: 10.1016/j.tplants.2007.08.003

  10. Re DA, Capella M, Bonaventure G, Chan RL. Arabidopsis AtHB7 and AtHB12 evolved divergently to fine tune processes associated with growth and responses to water stress. BMC Plant Biol 2014; 14: 150. doi: 10.1186/1471-2229-14-150

  11. Olsson AS, Engstrom P, Soderman E. The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis. Plant Mol Biol 2004; 55(5): 663–77. doi: 10.1007/s11103-004-1581-4

  12. Zhao Y, Ma Q, Jin X, Peng X, Liu J, Deng L, et al. A novel maize homeodomain-leucine zipper (HD-Zip) I gene, Zmhdz10, positively regulates drought and salt tolerance in both rice and Arabidopsis. Plant Cell Physiol 2014; 55(6): 1142–56. doi: 10.1093/pcp/pcu054

  13. Changfu Z, Qingjie Y, Xiuzhen N, Chao B, Yanmin S, Lianxuan S, et al. Cloning and functional analysis of the promoters that upregulate carotenogenic gene expression during flower development in Gentiana lutea. Physiol Plant 2014; 150(4): 493–504. doi: 10.1111/ppl.12129

  14. Kato S, Tanno Y, Takaichi S, Shinomura T. Low temperature stress alters the expression of phytoene desaturase genes (crtP1 and crtP2) and ζ-carotene desaturase gene (crtQ) of Euglena gracilis and the cellular carotenoid content. Plant Cell Physiol 2018; 60(2): 274–84. doi: 10.1093/pcp/pcy208

  15. Omoni AO, Aluko RE. The anti-carcinogenic and anti-atherogenic effects of lycopene: a review. Trends Food Sci Technol 2005; 16(8): 344–50. doi: 10.1016/j.tifs.2005.02.002

  16. Fraser PD, Bramley PM. The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 2004; 43(3): 228–65. doi: 10.1016/j.plipres.2003.10.002

  17. Krinsky NI, Johnson EJ. Carotenoid actions and their relation to health and disease. Mol Aspects Med 2005; 26(6): 459–516. doi: 10.1016/j.mam.2005.10.001

  18. Stahl W, Sies H. Antioxidant activity of carotenoids. Mol Aspects Med 2003; 24(6): 345–51. doi: 10.1016/S0098-2997(03)00030-X

  19. Cazzonelli CI. Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 2011; 38(11): 833–47. doi: 10.1071/fp11192

  20. Bertram JS. Carotenoids and human health. Hawaii Med J 2002; 61(4): 77–8. doi: 10.1016/j.phrs.2007.01.012

  21. Fiedor J, Burda K. Potential role of carotenoids as antioxidants in human health and disease. Nutrients 2014; 6(2): 466–88. doi: 10.3390/nu6020466

  22. Kró M, Maxwell DP, Huner NPA. Exposure of dunaliella salina to low temperature mimics the high light-induced accumulation of carotenoids and the carotenoid binding protein (Cbr). Plant Cell Physiol 1997; 38(2): 213–16. doi: 10.1093/oxfordjournals.pcp.a029155

  23. Zhou J, Hunter DA, Lewis DH, McManus MT, Zhang H. Insights into carotenoid accumulation using VIGS to block different steps of carotenoid biosynthesis in petals of California poppy. Plant Cell Rep 2018; 37(9): 1311–23. doi: 10.1007/s00299-018-2314-5

  24. Brandt R, Cabedo M, Xie Y, Wenkel S. Homeodomain leucine-zipper proteins and their role in synchronizing growth and development with the environment. J Integr Plant Biol 2014; 56(6): 518–26. doi: 10.1111/jipb.12185

  25. Jiang Y, Liu C, Yan D, Wen X, Liu Y, Wang H, et al. MdHB1 down-regulation activates anthocyanin biosynthesis in the white-fleshed apple cultivar ‘Granny Smith’. J Exp Bot 2017; 68(5): 1055–69. doi: 10.1093/jxb/erx029

  26. Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D. A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J 2008; 55(2): 301–10. doi: 10.1111/j.1365-313X.2008.03505.x

  27. Manavella PA, Dezar CA, Bonaventure G, Baldwin IT, Chan RL. HAHB4, a sunflower HD-Zip protein, integrates signals from the jasmonic acid and ethylene pathways during wounding and biotic stress responses. Plant J 2008; 56(3): 376–88. doi: 10.1111/j.1365-313X.2008.03604.x

  28. Sun R-Z, Pan Q-H, Duan C-Q, Wang J. Light response and potential interacting proteins of a grape flavonoid 3′-hydroxylase gene promoter. Plant Physiol Biochem 2015; 97: 70–81. doi: 10.1016/j.plaphy.2015.09.016

  29. Zhang F, Zuo K, Zhang J, Liu X, Zhang L, Sun X, et al. An L1 box binding protein, GbML1, interacts with GbMYB25 to control cotton fibre development. J Exp Bot 2010; 61(13): 3599–613. doi: 10.1093/jxb/erq173

  30. Lu P, Zhang C, Liu J, Liu X, Jiang G, Jiang X, et al. RhHB1 mediates the antagonism of gibberellins to ABA and ethylene during rose (Rosa hybrida) petal senescence. Plant J Cell Mol Biol 2014; 78(4): 578–90. doi: 10.1111/tpj.12494

  31. Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 1999; 11(7): 1217–26. doi: 10.1105/tpc.11.7.1217

  32. Eva H, Olsson ASB, Henrik J, Henrik J, Johannes H, Peter EM, et al. Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 2005; 139(1): 509–18. doi: 10.1104/pp.105.063461

  33. Lee YH, Chun JY. A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol Biol 1998; 37(2): 377–84. doi: 10.1023/a:1006084305012

  34. Wang J-E, Li D-W, Zhang Y-L, Zhao Q, He Y-M, Gong Z-H. Defence responses of pepper (Capsicum annuum L.) infected with incompatible and compatible strains of Phytophthora capsici. Eur J Plant Pathol 2013; 136(3): 625–38. doi: 10.1007/s10658-013-0193-8

  35. Tian SL, Li L, Chai WG, Shah SN, Gong ZH. Effects of silencing key genes in the capsanthin biosynthetic pathway on fruit color of detached pepper fruits. BMC Plant Biol 2014; 14(1): 314. doi: 10.1186/s12870-014-0314-3

  36. Yu C, Zhan Y, Feng X, Huang ZA, Sun C. Identification and expression profiling of the auxin response factors in Capsicum annuum L. under abiotic stress and hormone treatments. Int J Mol Sci 2017; 18(12): 2719. doi: 10.3390/ijms18122719

  37. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998; 16(6): 735–43. doi: 10.1046/j.1365-313x.1998.00343.x

  38. Cabello JV, Arce AL, Chan RL. The homologous HD-Zip I transcription factors HaHB1 and AtHB13 confer cold tolerance via the induction of pathogenesis-related and glucanase proteins. Plant J Cell Mol Biol 2012; 69(1): 141–53. doi: 10.1111/j.1365-313X.2011.04778.x

  39. Ali M, Luo DX, Khan A, Haq SU, Gai WX, Zhang HX, et al. Classification and genome-wide analysis of chitin-binding proteins gene family in pepper (Capsicum annuum L.) and transcriptional regulation to phytophthora capsici, abiotic stresses and hormonal applications. Int J Mol Sci 2018; 19(8): 2216. doi: 10.3390/ijms19082216

  40. Wang JE, Li DW, Gong ZH, Zhang YL. Optimization of virus-induced gene silencing in pepper (Capsicum annuum L.). Genet Mol Res GMR 2013; 12(3): 2492–506. doi: 10.4238/2013.July.24.4

  41. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR. Method 2002; 25(4): 402–8. doi: 10.1006/meth.2001.1262

  42. Porra RJ, Thompson WA, Kriedemann PE. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimbiophysacta 1989; 975(3): 384–94. doi: 10.1016/s0005-2728(89)80347-0

  43. Wilson MF. A rapid method for the separation and quantification of simple phenolic acids in plant material using high-performance liquid chromatography. J Chromatogr A 1985; 346(346): 440–5. doi: 10.1016/S0021-9673(00)90538-7

  44. Dionisio-Sese ML, Tobita S. Antioxidant responses of rice seedlings to salinity stress. Plant Sci 1998; 135(1): 1–9. doi: 10.1016/S0168-9452(98)00025-9

  45. Beers RF, Jr., Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 1952; 195(1): 133–40. doi: 10.1016/S0074-7696(08)60016-9

  46. Flohé L, Günzler WA. Assays of glutathione peroxidase. Methods Enzymol 1984; 105(1): 114–21. doi: 10.1016/S0076-6879​(84)05015-1

  47. Emanuelsson O, von Heijne G. Prediction of organellar targeting signals. Biochim Biophys Acta 2001; 1541(1–2): 114–19. doi: 10.1016/s0167-4889(01)00145-8

  48. Jing-hao J, Min W, Huai-xia Z, Abid K, Ai-min W, De-xu L, et al. Genome-wide identification of the AP2/ERF transcription factor family in pepper (Capsicum annuum L.). Genome 2018;(5):gen-2018-0036. doi: 10.1139/gen-2018-0036

  49. Su Y, Xu L, Wang S, Wang Z, Yang Y, Chen Y, et al. Identification, phylogeny, and transcript of chitinase family genes in sugarcane. Sci Rep 2015; 5: 10708. doi: 10.1038/srep10708

  50. Szymańska R, Ślesak I, Orzechowska A, Kruk J. Physiological and biochemical responses to high light and temperature stress in plants. Environ Exp Bot 2017; 139: 165–77. doi: 10.1016/j.envexpbot.2017.05.002

  51. Schenck CA, Nadella V, Clay SL, Lindner J, Abrams Z, Wyatt SE. A proteomics approach identifies novel proteins involved in gravitropic signal transduction. Am J Bot 2013; 100(1): 194–202. doi: 10.3732/ajb.1200339

  52. Esmon CA, Pedmale UV, Liscum E. Plant tropisms: providing the power of movement to a sessile organism. Int J Dev Biol 2005; 49(5–6): 665–74. doi: 10.1387/ijdb.052028ce

  53. Uarrota VG, Severino RB, Maraschin M, eds. Abstract: maize landraces (Zea mays L.): a new prospective source for secondary metabolite production. Int Conf Image Inform Process 2011; 6(3): 218–26. doi: 10.1109/ICIIP.2011.6108925

  54. Lado J, Rodrigo M, Cronje P, Zacarías L. Involvement of lycopene in the induction of tolerance to chilling injury in grapefruit. Postharvest Biol Technol 2015; 100: 176–86. doi: 10.1016/j.postharvbio.2014.10.002

  55. Lado J, Rodrigo M, Climent MF, Gómez-Cadenas A, Zacarías L. Implication of the antioxidant system in chilling injury tolerance in the red peel of grapefruit. Postharvest Biol Technol 2016; 111: 214–23. doi: 10.1016/j.postharvbio.2015.09.013

  56. Landrum JT. Reactive oxygen and nitrogen species in biological systems: reactions and regulation by carotenoids. Carotenoids and Human Health: Springer. Totowa, NJ: Humana Press; 2013, pp. 57–101.

  57. Esteban R, Moran JF, Becerril JM, García-Plazaola JI. Versatility of carotenoids: an integrated view on diversity, evolution, functional roles and environmental interactions. Environ Exp Bot 2015; 119: 63–75. doi: 10.1016/j.envexpbot.2015.04.009

  58. Zou L-P, Sun X-H, Zhang Z-G, Liu P, Wu J-X, Tian C-J, et al. Leaf rolling controlled by the homeodomain leucine zipper class IV gene Roc5 in rice. Plant Physiol 2011; 156(3): 1589–602. doi: 10.1104/pp.111.176016

  59. Shin D, Koo YD, Lee J, Lee H-J, Baek D, Lee S, et al. Athb-12, a homeobox-leucine zipper domain protein from Arabidopsis thaliana, increases salt tolerance in yeast by regulating sodium exclusion. Biochem Biophys Res Commun 2004; 323(2): 534–40. doi: 10.1016/j.bbrc.2004.08.127

  60. Shao J, Haider I, Xiong L, Zhu X, Hussain RMF, Overnas E, et al. Functional analysis of the HD-Zip transcription factor genes Oshox12 and Oshox14 in rice. PLoS One 2018; 13(7): e0199248. doi: 10.1371/journal.pone.0199248

  61. Gao S, Xu F, Wei W, Chu C. Rice HOX12 regulates panicle exsertion by directly modulating the expression of elongated uppermost internode1. Plant Cell 2016; 28: 680–95. doi: 10.1105/tpc.15.01021

  62. Zhang S, Haider I, Kohlen W, Jiang L, Bouwmeester H, Meijer AH, et al. Function of the HD-Zip I gene Oshox22 in ABA-mediated drought and salt tolerances in rice. Plant Mol Biol 2012; 80(6): 571–85. doi: 10.1007/s11103-012-9967-1

  63. Wang QQ, Zha KY, Chai WB, Wang Y, Liu B, Jiang HY, et al. Functional analysis of the HD-Zip I gene ZmHDZ1 in ABA-mediated salt tolerance in rice. J Plant Biol 2017; 60(2): 207–14. doi: 10.1007/s12374-016-0413-9

  64. Tao N, Wang C, Xu J, Cheng Y. Carotenoid accumulation in postharvest ‘Cara Cara’ navel orange (Citrus sinensis Osbeck) fruits stored at different temperatures was transcriptionally regulated in a tissue-dependent manner. Plant Cell Rep 2012; 31(9): 1667–76. doi: 10.1007/s00299-012-1279-z

  65. Cazzonelli CI, Pogson BJ. Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 2010; 15(5): 266–74. doi: 10.1016/j.tplants.2010.02.003

  66. Gu Z, Chen D, Han Y, Chen Z, Gu F. Optimization of carotenoids extraction from Rhodobacter sphaeroides. LWT Food Sci Technol 2008; 41(6): 1082–8. doi: 10.1016/j.lwt.​2007.07.005

  67. Henrik J, Yan W, Johannes H, Peter EM. The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol 2003; 51(5): 719–29. doi: 10.1023/A:1022567625228

  68. Axel H, Thomas H, Martin L, Beat HH, Erwin G. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. Embo J 2002; 21(12): 3029–38. doi: 10.1093/emboj/cdf316

  69. Rodriguez-Uribe L, Guzman I, Rajapakse W, Richins RD, O’Connell MA. Carotenoid accumulation in orange-pigmented Capsicum annuum fruit, regulated at multiple levels. J Exp Bot 2012; 63(1): 517–26. doi: 10.1093/jxb/err302

  70. Castrillo M, Luque EM, Pardo-Medina J, Limón MC, Corrochano LM, Avalos J. Transcriptional basis of enhanced photoinduction of carotenoid biosynthesis at low temperature in the fungus Neurospora crassa. Res Microbiol 2017; 169(2): 78–89. doi: 10.1016/j.resmic.2017.11.003

  71. Rugkong A, McQuinn R, Giovannoni JJ, Rose JKC, Watkins CB. Expression of ripening-related genes in cold-stored tomato fruit. Postharvest Biol Technol 2011; 61(1): 1–14. doi: 10.1016/j.postharvbio.2011.02.009

  72. DellaPenna D, Pogson BJ. Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 2006; 57: 711–38. doi: 10.1146/annurev.arplant.56.032604.144301

  73. Sun WH, Verhoeven AS, Bugos RC, Yamamoto HY. Suppression of zeaxanthin formation does not reduce photosynthesis and growth of transgenic tobacco under field conditions. Photosynth Res 2001; 67(1–2): 41–50. doi: 10.1023/a:1010636511935

  74. Schwarz N, Armbruster U, Iven T, BrãCkle L, Melzer M, Feussner I, et al. Tissue-specific accumulation and regulation of zeaxanthin epoxidase in Arabidopsis reflect the multiple functions of the enzyme in plastids. Plant Cell Physiol 2015; 56(2): 346–57. doi: 10.1093/pcp/pcu167

  75. Niyogi KK, Shih C, Chow WS, Pogson BJ, Dellapenna D, Björkman O. Photoprotection in a zeaxanthin and lutein-deficient double mutant of Arabidopsis. Photosynth Res 2001; 67(1–2): 139–45. doi: 10.1023/a:1010661102365

  76. Zhang Z, Wang Y, Chang L, Zhang T, An J, Liu Y, et al. MsZEP, a novel zeaxanthin epoxidase gene from alfalfa (Medicago sativa), confers drought and salt tolerance in transgenic tobacco. Plant Cell Rep 2016; 35(2): 439–53. doi: 10.1007/s00299-015-1895-5

  77. Duan J, Li J, Guo S, Kang Y. Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 2008; 165(15): 1620–35. doi: 10.1016/j.jplph.2007.11.006

  78. Groppa MD, Benavides MP. Polyamines and abiotic stress: recent advances. Amino Acids 2008; 34(1): 35–45. doi: 10.1007/s00726-007-0501-8

  79. Suzuki N, Koussevitzky S, Mittler R, Miller G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 2012; 35(2): 259–70. doi: 10.1111/j.1365-3040.​2011.02336.x

  80. Dong HL, Lee CB. Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 2000; 159(1): 75–85. doi: 10.1016/s0168-9452(00)00326-5

  81. Meng G, Yu-Fei Z, Jin-Ping L, Lin C, Wei-Guo C, Zhen-Hui G, et al. Characterization of CaHsp70-1, a pepper heat-shock protein gene in response to heat stress and some regulation exogenous substances in Capsicum annuum L. Int J Mol Sci 2014; 15(11): 19741–59. doi: 10.3390/ijms151119741

  82. Layrisse M, García-Casal MN, Solano L, Barón MA, Arguello F, Llovera D, et al. Vitamin A reduces the inhibition of iron absorption by phytates and polyphenols. Food Nutr Bull 1998; 19(19) :3–5(3). doi: 10.1177/156482659801900101

  83. Li Q, Yu B, Gao Y, Dai AH, Bai JG. Cinnamic acid pretreatment mitigates chilling stress of cucumber leaves through altering antioxidant enzyme activity. J Plant Physiol 2011; 168(9): 927–34. doi: 10.1016/j.jplph.2010.11.025

  84. Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, et al. Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 2012; 35(2): 281–95. doi: 10.1111/j.1365-3040.2011.02310.x

  85. Naydenov NG, Sakina K, Maryna S, Chiharu N. Profiling of mitochondrial transcriptome in germinating wheat embryos and seedlings subjected to cold, salinity and osmotic stresses. Genes Genet Syst 2010; 85(1): 31. doi: 10.1266/ggs.85.31

  86. Oidaira H, Sano S, Koshiba T, Ushimaru T. Enhancement of antioxidative enzyme activities in chilled rice seedlings. J Plant Physiol 2000; 156(5–6): 811–13. doi: 10.1016/S0176-1617(00)80254-0

  87. Bajji M, Kinet JM, Lutts S. The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul 2002; 36(1): 61–70. doi: 10.1023/a:1014732714549

  88. Gusta LV, Benning NT, Wu G, Luo X, Liu X, Gusta ML, et al. Superoxide dismutase: an all-purpose gene for agri-biotechnology. Mol Breed 2009; 24(2): 103–15. doi: 10.1007/s11032-009-9274-y

  89. Dang FF, Wang YN, Yu L, Eulgem T, Lai Y, Liu ZQ, et al. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ 2013; 36(4): 757–74. doi: 10.1111/pce.12011

  90. O’Kane D, Gill V, Boyd P, Burdon R. Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 1996; 198(3): 371–7. doi: 10.1007/bf00620053

  91. Hur YS, Um JH, Kim S, Kim K, Park HJ, Lim JS, et al. Arabidopsis thaliana homeobox 12 (ATHB12), a homeodomain-leucine zipper protein, regulates leaf growth by promoting cell expansion and endoreduplication. New Phytol 2015; 205(1): 316–28. doi: 10.1111/nph.12998

  92. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, et al. Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 2000; 42(4): 657–65. doi: 10.1023/a:1006321900483

  93. Ding Z, Li S, An X, Liu X, Qin H, Wang D. Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genom 2009; 36(1): 17–29. doi: 10.1016/S1673-8527(09)60003-5

  94. Yong HC, Sun JS, Kim BG, Pandey GK, Cho JS, Kim KN, et al. Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis. Mol Cells 2010; 29(2): 159–65. doi: 10.1007/s10059-010-0025-z

  95. Huang LJ, Cheng GX, Khan A, Wei AM, Yu QH, Yang SB, et al. CaHSP16.4, a small heat shock protein gene in pepper, is involved in heat and drought tolerance. Protoplasma 2019; 256(1): 39–51. doi: 10.1007/s00709-018-1280-7

  96. Chen Q, Yang G. Signal function studies of ROS, especially RBOH-dependent ROS, in plant growth, development and environmental stress. J Plant Growth Regul 2019; 39(1): 157–71. doi: 10.1007/s00344-019-09971-4

  97. Zhang M, Smith JA, Harberd NP, Jiang C. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol 2016; 91(6): 651–9. doi: 10.1007/s11103-016-0488-1

  98. Baxter A, Mittler R, Suzuki N. ROS as key players in plant stress signalling. J Exp Bot 2014; 65(5): 1229–40. doi: 10.1093/jxb/ert375

Published
2020-12-28
How to Cite
Zhang R.-X., Zhu W.-C., Cheng G.-X., Yu Y.-N., Li Q.-H., ul Haq S., Said F., & Gong Z.-H. (2020). A novel gene, <em>CaATHB-12</em>, negatively regulates fruit carotenoid content under cold stress in <em>Capsicum annuum</em&gt;. Food & Nutrition Research, 64. https://doi.org/10.29219/fnr.v64.3729
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Original Articles