Abstract
The desiccation tolerant desert moss Syntrichia caninervis is a potential source for genetic element that could be utilized for crop improvement for drought tolerance. An ABSCISIC ACID INSENSITIVE3 (ABI3) transcriptional factor, that plays critical role in the regulation ABA influenced dehydration tolerance, has been isolated, characterized and overexpressed in transgenic Arabidopsis. The ScABI3 gene encodes a highly conserved protein structure typical of ABI3 genes from other plant sources. It is induced by dehydration, rehydration, and cold. It is localized in the nuclei of transiently transformed tobacco endodermal cells and exhibits transactivation activity. Ectopic expression of ScABI3 in Arabidopsis enhanced salinity and osmotic stress tolerance, and alters the responsiveness of several abiotic stress induced genes. These results suggest that ScABI3 has promise as a possible target gene for abiotic stress tolerance improvement strategies.
Similar content being viewed by others
References
Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61 61:651–679. https://doi.org/10.1146/annurev-arplant-042809-112122
Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, Northey JGB, McCourt P, Samuel MA (2013) ABI3 controls embryo degreening through Mendel’s I locus. Proc Natl Acad Sci USA 110(40):E3888–E3894. https://doi.org/10.1073/pnas.1308114110
Finkelstein RR, Rock CD (2002) Abscisic acid biosynthesis and response. Arabidopsis Book. Arabidopsis Book. The American Society of Plant Biologists publisher, Rockville, p e0058. https://doi.org/10.1199/tab.0058
Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53(372):1249–1254. https://doi.org/10.1093/jexbot/53.372.1249
Gao B, Zhang D, Li X, Yang H, Wood AJ (2014a) De novo assembly and characterization of the transcriptome in the desiccation-tolerant moss Syntrichia caninervis. BMC Res Notes 7(1):1–12. https://doi.org/10.1186/1756-0500-7-490
Gao DY, Xu ZS, He Y, Sun YW, Ma YZ, Xia LQ (2014b) Functional analyses of an E3 ligase gene AIP2 from wheat in Arabidopsis revealed its roles in seed germination and pre-harvest sprouting. J Integr Plant Biol 56(5):480–491. https://doi.org/10.1111/jipb.12135
Gaweł S, Wardas M, Niedworok E, Wardas P (2004) Malondialdehyde (MDA) as a lipid peroxidation marker. Wiadomosci lekarskie (Warsaw: 1960) 57(9–10):453–455
Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87–96. https://doi.org/10.1016/S0076-6879(02)50957-5
Hartung W (2010) The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37(9):806–812. https://doi.org/10.1071/Fp10058
Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303(5913):179–180. https://doi.org/10.1038/303179a0
Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud PF, Pan A, Quatrano RS (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327(5965):546. https://doi.org/10.1126/science.1183672
Komatsu K, Nishikawa Y, Ohtsuka T, Taji T, Quatrano RS, Tanaka S, Sakata Y (2009) Functional analyses of the ABI1-related protein phosphatase type 2C reveal evolutionarily conserved regulation of abscisic acid signaling between Arabidopsis and the moss Physcomitrella patens. Plant Mol Biol 70(3):327–340. https://doi.org/10.1007/s11103-009-9476-z
Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9(4):299–306. https://doi.org/10.1093/bib/bbn017
Li Y, Wang ZB, Xu TH, Tu WF, Liu C, Zhang YM, Yang CH (2010) Reorganization of photosystem II is involved in the rapid photosynthetic recovery of desert moss Syntrichia caninervis upon rehydration. J Plant Physiol 167(16):1390–1397. https://doi.org/10.1016/j.jplph.2010.05.028
Li X, Zhang D, Li H, Gao B, Yang H, Zhang Y, Wood AJ (2015) Characterization of reference genes for RT-qPCR in the desert moss Syntrichia caninervis in response to abiotic stress and desiccation/rehydration. Front Plant Sci 6:38. https://doi.org/10.3389/fpls.2015.00038
Li XS, Zhang DY, Gao B, Liang YQ, Yang HL, Wang YC, Wood AJ (2017) Transcriptome-wide identification, classification, and characterization of AP2/ERF family genes in the desert moss Syntrichia caninervis. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00262
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lopez-Molina L, Mongrand B, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32(3):317–328. https://doi.org/10.1046/j.1365-313X.2002.01430.x
Marella HH, Quatrano RS (2007) The B2 domain of VIVIPAROUS1 is bi-functional and regulates nuclear localization and transactivation. Planta 225(4):863–872. https://doi.org/10.1007/s00425-006-0398-6
Marella HH, Sakata Y, Quatrano RS (2006) Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3-like genes from Physcomitrella patens. Plant J 46(6):1032–1044. https://doi.org/10.1111/j.1365-313X.2006.02764.x
Mccarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK (1991) The viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66(5):895–905. https://doi.org/10.1016/0092-8674(91)90436-3
Mittal A, Gampala SSL, Ritchie GL, Payton P, Burke JJ, Rock CD (2014) Related to ABA-insensitive3(ABI3)/viviparous1 and AtABI5 transcription factor coexpression in cotton enhances drought stress adaptation. Plant Biotechnol J 12(5):578–589. https://doi.org/10.1111/pbi.12162
Nakamura S, Lynch TJ, Finkelstein RR (2001) Physical interactions between ABA response loci of Arabidopsis. Plant J 26(6):627–635. https://doi.org/10.1046/j.1365-313x.2001.01069.x
Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151(1):85–100. https://doi.org/10.1023/A:1026550808557
Oliver MJ, Dowd SE, Zaragoza J, Mauget SA, Payton PR (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genom. https://doi.org/10.1186/1471-2164-5-89
Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45(5):788–799. https://doi.org/10.1093/icb/45.5.788
Ooms JJJ, Leonkloosterziel KM, Bartels D, Koornneef M, Karssen CM (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana—a comparative-study using abscisic acid-insensitive abi3 mutants. Plant Physiol 102(4):1185–1191. https://doi.org/10.1104/pp.102.4.1185
Parcy F, Giraudat J (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant J 11(4):693–702. https://doi.org/10.1046/j.1365-313X.1997.11040693.x
Parcy F, Valon C, Raynal M, Gaubiercomella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6(11):1567. https://doi.org/10.1105/tpc.6.11.1567
Pilate G, Sossountzov L, Miginiac E (1989) Hormone levels and apical dominance in the aquatic fern Marsilea drummondii A. Br. Plant Physiol 90(3):907. https://doi.org/10.1104/pp.90.3.907
Proctor MCF, Pence VC, Black M, Pritchard HW (2002) Vegetative tissues: bryophytes, vascular resurrection plants and vegetative propagules. Desiccation Surv Plants.https://doi.org/10.1079/9780851995342.0207
Rock CD, Sakata Y, Quatrano RS (2009) Stress signaling I: the role of abscisic acid (ABA). Springer, Dordrecht
Rohde A, Kurup S, Holdsworth M (2000) ABI3 emerges from the seed. Trends Plant Sci 5(10):418–419. https://doi.org/10.1016/S1360-1385(00)01736-2
Rohde A, Prinsen E, De Rycke R, Engler G, Van Montagu M, Boerjan W (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell 14(8):1885–1901. https://doi.org/10.1105/tpc.003186
Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1(4):2019–2025. https://doi.org/10.1038/nprot.2006.286
Suzuki M, McCarty DR (2008) Functional symmetry of the B3 network controlling seed development. Curr Opin Plant Biol 11(5):548–553. https://doi.org/10.1016/j.pbi.2008.06.015
Suzuki M, Kao CY, McCarty DR (1997) The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 9(5):799–807. https://doi.org/10.1105/tpc.9.5.799
Takezawa D, Komatsu K, Sakata Y (2011) ABA in bryophytes: how a universal growth regulator in life became a plant hormone? J Plant Res 124(4):437–453. https://doi.org/10.1007/s10265-011-0410-5
Tamminen I, Makela P, Heino P, Palva ET (2001) Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. Plant J 25(1):1–8. https://doi.org/10.1046/j.1365-313x.2001.00927.x
Tougane K, Komatsu K, Bhyan SB, Sakata Y, Ishizaki K, Yamato KT, Kohchi T, Takezawa D (2010) Evolutionarily conserved regulatory mechanisms of abscisic acid signaling in land plants: characterization of ABSCISIC ACID INSENSITIVE1-like type 2C protein phosphatase in the liverwort Marchantia polymorpha. Plant Physiol 152(3):1529–1543. https://doi.org/10.1104/pp.110.153387
Werner O, Espin RMR, Bopp M, Atzorn R (1991) Abscisic-acid-induced drought tolerance in Funaria-Hygrometrica Hedw. Planta 186(1):99–103. https://doi.org/10.1007/BF00201503
Wood AJ (2007) The nature and distribution of vegetative desiccation-tolerance in hornworts, liverworts and mosses. Bryologist 110(2):163–177
Wood AJ, Oliver MJ (2004) Molecular biology and genomics of the desiccation tolerant moss Tortula ruralis. Springer, Dordrecht
Yotsui I, Saruhashi M, Kawato T, Taji T, Hayashi T, Quatrano RS, Sakata Y (2013) ABSCISIC ACID INSENSITIVE3 regulates abscisic acid-responsive gene expression with the nuclear factor Y complex through the ACTT-core element in Physcomitrella patens. New Phytol 199(1):101–109. https://doi.org/10.1111/nph.12251
Yotsui I, Serada S, Naka T, Saruhashi M, Taji T, Hayashi T, Quatrano RS, Sakata Y (2016) Large-scale proteome analysis of abscisic acid and ABSCISIC ACID INSENSITIVE3-dependent proteins related to desiccation tolerance in Physcomitrella patens. Biochem Biophys Res Commun 471(4):589–595. https://doi.org/10.1016/j.bbrc.2016.02.024
Zeng Y, Raimondi N, Kermode AR (2003) Role of an ABI3 homologue in dormancy maintenance of yellow-cedar seeds and in the activation of storage protein and Em gene promoters. Plant Mol Biol 51(1):39–49. https://doi.org/10.1023/A:1020762304937
Zhang XR, Garreton V, Chua NH (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Gene Dev 19(13):1532–1543. https://doi.org/10.1101/gad.1318705
Zhang YM, Chen J, Wang L, Wang XQ, Gu ZH (2007) The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China. J Arid Environ 68(4):599–610. https://doi.org/10.1016/j.jaridenv.2006.06.012
Zheng YP, Xu M, Zhao JC, Zhang BC, Bei SQ, Hao LH (2011) Morphological adaptations to drought and reproductive strategy of the moss Syntrichia caninervis in the Gurbantunggut Desert, China. Arid Land Res Manag 25(2):116–127. https://doi.org/10.1080/15324982.2011.554956
Acknowledgements
This work was supported by the scientific service project of CAS (TSS-2015-014-FW-4-3) and NSFC-Xinjiang talent youth project (No. U1403302). We are grateful to Dr. Melvin J. Oliver at University of Missouri for critical comments and valuable suggestions to the manuscript.
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments: YGZ, DYZ and KYG. Conducted the experiments: YGZ and XJL. Analyzed the data: KCZ. Contributed to the writing of the manuscript: YGZ and DYZ.
Corresponding author
Additional information
Communicated by Sergio J. Ochatt.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, Y., Liu, X., Zhang, K. et al. An ABSCISIC ACID INSENSITIVE3-like gene from the desert moss Syntrichia caninervis confers abiotic stress tolerance and reduces ABA sensitivity. Plant Cell Tiss Organ Cult 133, 417–435 (2018). https://doi.org/10.1007/s11240-018-1394-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-018-1394-9