Skip to main content
SpringerLink
Log in

Overexpression of ATHG1/AHL23 and ATPG3/AHL20, Arabidopsis AT-hook motif nuclear-localized genes, confers salt tolerance in transgenic Zoysia japonica

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Zoysia japonica Steud. is a native turfgrass in the Korean peninsula and is used worldwide. Abnormal conditions of soil salinity inhibit plant growth and adversely affect the quality of the turfgrass. AT-hook motif nuclear-localized (AHL) family proteins known to co-regulate the transcription of genes as a chromatin remodeling factor play a role in plant developmental processes and stress responses. In this study, AT-Hook Protein of Genomine 1 (ATHG1)/AT-Hook motif nuclear-Localized protein 23 (AHL23) and AT-hook Protein of Genomine 3 (ATPG3)/AT-Hook motif nuclear-Localized protein 20 (AHL20), two AHL genes from A. thaliana, were transformed into Z. japonica under the control of a constitutive ubiquitin promoter. Southern blot analysis proved that ATHG1/AHL23 and ATPG3/AHL20 were introduced into the ATHG1/AHL23-transgenic plants and ATPG3/AHL20-transgenic plants, respectively. Overexpression of each ATHG1/AHL23 and ATPG3/AHL20 in all of the transgenic plants was confirmed by quantitative real-time PCR (qRT-PCR). To evaluate a tolerant response to salt stress of the transgenic plants, 4 transgenic plants including ATHG1-overexpressing line 1 (ATHG1-OE1) and ATHG1-OE2, and ATPG3-overexpressing line 1 (ATPG3-OE1) and ATPG3-OE2 were selected, respectively. All the transgenic plants showed higher salt-tolerant phenotype with higher chlorophyll and lower malondialdehyde (MDA) contents under salt treatment, compared to the wild types. Also, under salt treatment, the transgenic plants revealed higher activities of catalase (CAT) and peroxidase (POD), reactive oxygen species (ROS)-scavenging enzymes, than those of the wild-type plant. These results suggest that overexpression of ATHG1/AHL23 or ATPG3/AHL20 belonging to the AHL gene family confers salt tolerance to the transgenic zoysiagrass plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods in Enzymol 105:121–126

    CAS  Google Scholar 

  • Ahanger MA, Akram NA, Ashraf M, Alyemeni MN, Wijaya L, Ahmad P (2017) Plant responses to environmental stresses-from gene to biotechnology. AoB Plants 9:1–17

    Google Scholar 

  • Ashraf M, Athar HR, Harris PJC, Kwon TR (2008) Some prospective strategies for improving crop salt tolerance. Adv Agron 97:45–110

    CAS  Google Scholar 

  • Bae TW, Vanjidorj E, Song SY, Nishiguchi S, Yang SS, Song IJ (2008) Environmental risk assessment of genetically engineered herbicide-tolerant Zoysia japonica. J Environ Qual 37:207–218

    CAS  PubMed  Google Scholar 

  • Bae EJ, Lee KS, Han EH, Lee SM, Lee DW (2013) Sod production and current status of cultivation management in Korea. Weed Truf Sci 2:95–99 (In Korean)

    Google Scholar 

  • Bishop EH, Kumar R, Luo F, Saski C, Sekhon RS (2019) Genome-wide identification, expression profiling and network analysis of AT-hook gene family in maize. Genomics 19:S0888–7543

    Google Scholar 

  • Braun JE, Huntzinger E, Fauser M, Izaurralde E (2011) GW182 proteins recruit cytoplasmic deadenylase complex to miRNA targets. Mol Cell 44:120–133

    CAS  PubMed  Google Scholar 

  • Cabot C, Sibole JV, Barcelo J, Poschenrieder C (2014) Lessons from crop plants struggling with salinity. Plant Sci 226:2–13

    CAS  PubMed  Google Scholar 

  • Cho HS, Lee DH, Jung HW, Oh SW, Kim HJ, Chung YS (2019) Evaluation of yield components from transgenic soybean overexpressing chromatin architecture-controlling ATPG8 and ATPG10 genes. Plant Breed Biotechnol 7:34–41

    Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Google Scholar 

  • Ding HD, Zhu XH, Zhu ZW, Yang SJ, Zha DS, Wu XX (2012) Amelioration of salt-induced oxidative stress in eggplant by application of 24-epibrassinolide. Biol Plant 56:767–770

    CAS  Google Scholar 

  • Elsheery NI, Cao KF (2008) Gas exchange, chlorophyll fluorescence, and osmotic adjustment in two mango cultivars under drought stress. Acta Physiol Plant 30:769–777

    CAS  Google Scholar 

  • Engelke MC, Anderson S (2003) Zoysiagrasses (Zoysia spp.). In: Casler MD, Duncan RR (eds) Turfgrass biology, genetics, and breeding. Wiley, Hoboken, pp 271–286

    Google Scholar 

  • Florina F, Giancarla V, Cerasela P, Sofia P (2013) The effect of salt stress on chlorophyll content in several Romanian tomato varieties. J Hortic For Biotechnol 17:363–367

    Google Scholar 

  • Gallavotti A, Malcomber S, Gaines C, Stanfield S, Whipple C, Kellogg E, Schmidt RJ (2011) BARREN STALK FASTIGIATE1 is an AT-hook protein required for the formation of maize ears. Plant Cell 23:1756–1771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ganesan M, Han YJ, Bae TW, Hwang OJ, Chandrasekhar T, Shin AY, Goh CH, Nishiguchi S, Song IJ, Lee HY, Kim JI, Song PS (2012) Overexpression of phytochrome A and its hyperactive mutant improves shade tolerance and turf quality in creeping bentgrass and zoysiagrass, a hyperactive mutant gene (S599A-PHYA). Planta 236:1135–1150

    CAS  PubMed  Google Scholar 

  • Guidi L, Tonini M, Soldatini GF (2000) Effects of high light and ozone fumigation on photosynthesis in Phaseolus vulgaris. Plant Physiol Biochem 38:717–725

    CAS  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Gen https://doi.org/10.1155/2014/701596

    Article  Google Scholar 

  • Gururani MA, Ganesan M, Song IJ, Han Y, Kim JI, Lee HY, Song PS (2015) Transgenic turfgrass expressing hyperactive Ser599Ala phytochrome A mutant exhibit abiotic stress tolerance. J Plant Growth Regul 35:11–21

    Google Scholar 

  • Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235

    CAS  PubMed  Google Scholar 

  • Holsters M, De Waele D, Depicker A, Messens E, Van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet 163:181–187

    CAS  PubMed  Google Scholar 

  • Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208–218

    CAS  Google Scholar 

  • Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24:2279–2303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu T, Yi H, Ju L, Fu J (2013) Stomatal and metabolic limitations to photosynthesis resulting from NaCl stress in perennial ryegrass genotypes differing in salt tolerance. J Am Soc Hortic Sci 138:350–357

    Google Scholar 

  • Huang B, DaCosta M, Jiang Y (2014) Research advances in mechanisms of turfgrass tolerance to abiotic stresses: from physiology to molecular biology. Crit Rev Plant Sci 33:141–189

    CAS  Google Scholar 

  • Jia QS, Zhu J, Xu XF, Lou Y, Zhang ZL, Zhang ZP, Yang ZN (2015) Arabidopsis AT-hook protein TEK positively regulates the expression of arabionogalactan proteins for nexine formation. Mol Plant 8:251–260

    CAS  PubMed  Google Scholar 

  • Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18:3015–3032

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kang G, Li G, Zheng B, Han Q, Wang C, Zhu Y, Guo T (2012) Proteomic analysis on salicylic acid-induced salt tolerance in common wheat seedlings [Triticum aestivum L.]. Biochim Biophys Acta 1824:1324–1333

    CAS  PubMed  Google Scholar 

  • Kim YH, Khan AL, Waqas M, Shahzad R, Lee IJ (2016) Silicon-mediated mitigation of wounding stress acts by up-regulating the rice antioxidant system. Cereal Res Commun 44:111–121

    CAS  Google Scholar 

  • Kim HJ, Cho HS, Pak JH, Kim KJ, Lee DH, Chung YS (2017) Overexpression of a chromatin architecture-controlling ATPG7 has positive effect on yield components in transgenic soybean. Plant Breed Biotechnol 5:237–242

    Google Scholar 

  • Kong W, Liu F, Zhang C, Zhang J, Feng H (2016) Non-destructive determination of malondialdehyde (MDA) distribution in oilseed rape leaves by laboratory scale NIR hyperspectral imaging. Sci Rep 6:35393

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kume A, Akitsu T, Nasahara KN (2018) Why is chlorophyll b only used in light-harvesting systems? J Plant Res 131(6):961–972

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee GJ, Carrow RN, Duncan RR (2005) Criteria for assessing salinity tolerance of the halophytic turfgrass seashore paspalum. Crop Sci 45:251–258

    CAS  Google Scholar 

  • Lee DH, Kim KJ, Lee IC, Kim DS (2011) ATHG1 protein having senescence delaying function and stress resisting function of plant and gene, and use of protein. PCT/KR2010/000767

  • Lee DH, Lee IC, Kim KJ, Kim DS, Park KM (2013) ATPG3 protein having ability to increase productivity, senescence delaying ability and ability for plants to resist stress, gene of ATPG3 protein, and use thereof. PCT/KR2013/001311

  • Li B, Kliebenstein DJ (2014) The AT-hook Motif-encoding Gene METABOLIC NETWORK MODULATOR 1 underlies natural variation in Arabidopsis primary metabolism. Front Plant Sci 5:415

    PubMed  PubMed Central  Google Scholar 

  • Li J, Pu L, Han M, Zhu M, Zhang R, Xiang Y (2014) Soil salinization research in China: advances and prospects. J Geogr Sci 24:943–960

    Google Scholar 

  • Li J, Ma J, Guo H, Zong J, Chen J, Wang Y, Li D, Li L, Wang J, Liu J (2018) Growth and physiological responses of two phenotypically distinct accessions of centipedegrass (Eremochloa Ophiuroides (Munnro) Hack.) to salt stress. Plant Physiol Biochem 126:1–10

    PubMed  Google Scholar 

  • Lim PO, Kim Y, Breeze E, Koo JC, Woo HR, Ryu JS, Park DH, Beynon J, Tabrett A, Buchanan-Wollaston V, Nam HG (2007) Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. Plant J 52:1140–1153

    CAS  PubMed  Google Scholar 

  • Lou Y, Xu XF, Zhu J, Gu JN, Blackmore S, Yang ZN (2014) The tapetal AHL family protein TEK determines nexine formation in the pollen wall. Nat Commun 5:3855

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu H, Zou Y, Feng N (2010) Overexpression of AHL20 negatively regulates defenses in Arabidopsis. J Integr Plant Biol 52:801–808

    CAS  PubMed  Google Scholar 

  • Marcum KB (2006) Use of saline and non-potable water in the turfgrass industry: constraints and developments. Agric Water Manag 80:132–146

    Google Scholar 

  • Matsushita A, Furumoto T, Ishida S, Takahashi Y (2007) AGF1, an AT-hook protein, is necessary for the negative feedback of AtGA3ox1 encoding GA 3-oxidase. Plant Physiol 143:1152–1162

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miransari M, Smith DL (2007) Overcoming the stressful effects of salinity and acidity on soybean [Glycine max (L.) Merr.] nodulation and yields using signal molecule genistein under field conditions. J Plant Nutr 30:1967–1992

    CAS  Google Scholar 

  • Ng KH, Yu H, Ito T (2009) AGAMOUS controls GIANT KILLER, a multifunctional chromatin modifier in reproductive organ patterning and differentiation. PLoS Biol 7:e100251

    Google Scholar 

  • Nxele X, Klein A, Ndimba B (2017) Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants. S Afr J Bot 108:261–266

    CAS  Google Scholar 

  • Oron G, DeMalach Y, Gillerman L, David I, Lurie S (2002) Effect of water salinity and irrigation technology on yield and quality of pears. Biosyst Eng 81:237–247

    Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) 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. Biochim Biophys Acta 975:384–394

    CAS  Google Scholar 

  • Putter J (1974) Methods of enzymatic analysis. In: Bergmeyer HU (ed) Peroxidase. Verlag Chemie-Academic Press, Weinheim, pp 685–690

    Google Scholar 

  • Rashotte AM, Carson SD, To JP, Kieber JJ (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132:1998–2011

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rengasamy P (2010) Soil processes affecting crop production in salt-affected soils. Funct Plant Biol 37:613–620

    Google Scholar 

  • Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh herbarium and mummified plant tissues. Plant Mol Biol 5:69–76

    CAS  PubMed  Google Scholar 

  • Shao F, Zhan L, Wilson LW LW, Qiu D (2018) Transcriptomic analysis of Betula halophila in response to salt stress. Int J Mol Sci 19:3412

    PubMed Central  Google Scholar 

  • Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669

    CAS  Google Scholar 

  • Street IH, Shah PK, Smith AM, Avery N, Neff MM (2008) The AT-hook-containing proteins SOB3/AHL29 and ESC/AHL27 are negative modulators of hypocotyl growth in Arabidopsis. Plant J 54(1):1–14

    CAS  PubMed  Google Scholar 

  • Suarez-Hernanderz AM, Vazquez-Angulo JC, Grimaldo-Juarez O, Cecena-Duran C, Gonzalez-Mendoza D, Bazante-Gonzalez I, Mendoza-Gomez A (2019) Production and quality of grafted watermelon in saline soil. Hortic Bras 37:215–220

    Google Scholar 

  • Toyama K, Bae CH, Kang JG, Lim YP, Adachi T, Riu KZ, Song PS, Lee HY (2003) Production of herbicide-tolerant zoysiagrass by Agrobacterium-mediated transformation. Mol Cells 16:19–27

    CAS  PubMed  Google Scholar 

  • Trenholm LE, Schlossberg MJ, Lee G, Park W, Geer SA (2000) An evaluation of multi-spectral responses on selected turfgrass specie. Int J Remote Sens 21:704–721

    Google Scholar 

  • Tunc-Ozdemir M, Miller G, Song L, Kim J, Sodek A, Koussevitzky S, Misra AN, Mittler R, Shintani D (2009) Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol 151:421–432

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uddin MDK, Juraimi AS (2013) Salinity tolerance turfgrass: history and prospects. World Sci J 2013:1–6

    Google Scholar 

  • Vom Endt D, Soares e Silva M, Kijne JW, Pasquali G, Memelink J (2007) Identification of a bipartite jasmonate-responsive promoter element in the Catharanthus roseus ORCA3 transcription factor gene that interacts specifically with AT-hook DNA-binding protein. Plant Physiol 144:1680–1689

    Google Scholar 

  • Wong MM, Bhaskara GB, Wen TN, Lin WD, Nguyen TT, Chong GL, Verslues PE (2019) Phosphoproteomics of Arabidopsis highly ABA-induced1 identifies AT-hook–like10 phosphorylation required for stress growth regulation. Proc Natl Acad Sci USA 116:2354

    CAS  PubMed  Google Scholar 

  • Xiao C, Chen F, Yu X, Lin C, Fu YF (2009) Over-expression of an AT-hook gene, AHL22, delays flowering and inhibits the elongation of the hypocotyl in Arabidopsis thaliana. Plant Mol Biol 71:39–50

    CAS  PubMed  Google Scholar 

  • Xu Y, Wang Y, Stroud H, Gu X, Sun B, Gan ES, Ng KH, Jacobsen SE, He Y, Ito T (2013) A matrix protein silences transposons and repeats through interaction with retinoblastoma-associated proteins. Curr Biol 23:345–350

    CAS  PubMed  Google Scholar 

  • Yin D, Liu X, Shi Z, Li D, Zhu L (2018) An AT-hook protein DEPRESSED PALEA1 physically interacts with the TCP family transcription factor RETARDED PALEA1 in rice. Biochem Biophys Res Commun 495:487–492

    CAS  PubMed  Google Scholar 

  • You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Front Plant Sci 6:1092

    PubMed  PubMed Central  Google Scholar 

  • Yun J, Kim YS, Jung JH, Seo PJ, Park CM (2012) The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J Biol Chem 287:15307–15316

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Fang Y, Ji Y, Jiang Z, Wang L (2013) Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afr J Bot 85:1–9

    Google Scholar 

  • Zhao J, Favero DS, Peng H, Neff MM (2013) Arabidopsis thaliana AHL family modulates hypocotyl growth redundantly by interacting with each other via the PPC/DUF296 domain. Proc Natl Acad Sci USA 110:E4688–E4697

    CAS  PubMed  Google Scholar 

  • Zhao J, Favero DS, Qiu J, Roalson EH, Neff MM (2014) Insights into the evolution and diversification of the AT-hook motif nuclear localized gene family in land plants. BMC Plant Biol 14:266

    PubMed  PubMed Central  Google Scholar 

  • Zhou J, Wang X, Lee JY, Lee JY (2013) Cell-to-cell movement of two interacting AT hook factors in Arabidopsis root vascular tissue patterning. Plant Cell 25:187–201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou L, Liu Z, Liu Y, Kong D, Li T, Yu S, Mei H, Xu X, Liu H, Chen L, Luo L (2016) A novel gene OsAHL1 improves both drought avoidance and drought tolerance in rice. Sci Rep 6:30264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuo ZF, Kang HG, Park MY, Jeong H, Sun HJ, Yang DH, Lee YE, Song PS, Lee HY (2019a) Overexpression of ICE1, a regulator of cold-induced transcriptome, confers cold tolerance to transgenic Zoysia japonica. J Plant Biol 62:137–146

    CAS  Google Scholar 

  • Zuo ZF, Kang HG, Park MY, Jeong H, Sun HJ, Song PS, Lee HY (2019b) Zoysia japonica MYC type transcription factor ZjICE1 regulates cold tolerance in transgenic Arabidopsis. Plant Sci 289:110254

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported in part by grants from Bio-Green 21 Program of Rural Development Administration (PJ01368501) and from Basic Science Research Program through the National Research Foundation of Korea (NRF) of the Ministry of Education (2019R1A6A1A11052070), Republic of Korea.

Author information

Authors and Affiliations

  1. Faculty of Biotechnology, Jeju National University, Jeju, 690-756, South Korea

    Ha-Na Jeong, Zhi-Fang Zuo & Hyo-Yeon Lee

  2. Subtropical Horticulture Research Institute, Jeju National University, Jeju, 690-756, South Korea

    Hyeon-Jin Sun, Pill-Soon Song, Hong-Gyu Kang & Hyo-Yeon Lee

  3. Quegenbiotech, Co., Ltd., Incheon, 429-931, South Korea

    Ha-Na Jeong

  4. Genomine Advanced Biotechnology Research Institute, Genomine Inc., Pohang, 37668, South Korea

    Dong Hee Lee

Authors
  1. Ha-Na Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hyeon-Jin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhi-Fang Zuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Hee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pill-Soon Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hong-Gyu Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hyo-Yeon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hong-Gyu Kang or Hyo-Yeon Lee.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeong, HN., Sun, HJ., Zuo, ZF. et al. Overexpression of ATHG1/AHL23 and ATPG3/AHL20, Arabidopsis AT-hook motif nuclear-localized genes, confers salt tolerance in transgenic Zoysia japonica. Plant Biotechnol Rep 14, 351–361 (2020). https://doi.org/10.1007/s11816-020-00606-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-020-00606-9

Keywords

Search

Navigation