biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 62:69-79, 2018 | DOI: 10.1007/s10535-017-0753-4

High irradiance sensitive phenotype of Arabidopsis hit2/xpo1a mutant is caused in part by nuclear confinement of AtHsfA4a

H.-Y. Huang1, K.-Y. Chang1, S.-J. Wu1,*
1 Department of Life Sciences, National Central University, Taoyuan City, Taiwan

In Arabidopsis, EXPORTIN1A (HIT2/XPO1A) and EXPORTIN1B (XPO1B) mediate the translocation of nuclear export sequence (NES)-bearing proteins from nucleus to cytoplasm. However, a mutation in HIT2/XPO1A but not in XPO1B induces sensitivity to high irradiance (HI). Arabidopsis thaliana heat stress elements A4a and A5 (AtHsfA4a and AtHsfA5) are involved in plant responses to HI and possess NESs; therefore, their nucleo-cytoplasmic partitioning was analyzed. In wild-type and xpo1b mutant cells, AtHsfA4a normally remained in the cytoplasm but became concentrated in the nucleus following exposure to HI, whereas AtHsfA5 was constitutively distributed in both cytoplasm and nucleus. However, in hit2/xpo1a mutant, AtHsfA4a and AtHsfA5 were always confined to the nucleus, regardless of the irradiance. Although AtHsfA4a can enhance the ability of plants to scavenge H2O2, and AtHsfA5 is a repressor of AtHsfA4a, athsfa5 but not athsfa4a mutant plants exhibited HI sensitivity. Additionally, athsfa4a plants expressing AtHsfA4aΔNES were sensitive to HI, but athsfa5 plants expressing AtHsfA5ΔNES were not. Meanwhile, hit2/athsfa4a double mutant was more tolerant to HI than hit2. These results indicate that both AtHsfA4a and AtHsfA5 were HIT2/XPO1A-specific substrates. Long-term accumulation of AtHsfA4a contributed to the hit2 HI-sensitive phenotype independent of the scavenging ability of H2O2, and the presence of AtHsfA5 could mitigate this adverse effect.

Keywords: exportin1 (XPO1); heat stress factor A4a; nuclear transport receptor
Subjects: mutant; high irradiance; heat stress factor; chlorophyll; fluorescence; hydrogen peroxide

Received: December 11, 2016; Revised: April 23, 2017; Accepted: April 25, 2017; Published: January 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Huang, H.-Y., Chang, K.-Y., & Wu, S.-J. (2018). High irradiance sensitive phenotype of Arabidopsis hit2/xpo1a mutant is caused in part by nuclear confinement of AtHsfA4a. Biologia plantarum62(1), 69-79. doi: 10.1007/s10535-017-0753-4
Download citation

Supplementary files

Download filebpl-201801-0007_S1.pdf

File size: 2.44 MB

References

  1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P., Stevenson, D.K., Zimmerman, J., Barajas, P., Cheuk, R., Gadrinab, C., Heller, C., Jeske, A., Koesema, E., Meyers, C.C., Parker, H., Prednis, L., Ansari, Y., Choy, N., Deen, H., Geralt, M., Hazari, N., Hom, E., Karnes, M., Mulholland, C., Ndubaku, R., Schmidt, I., Guzman, P., Aguilar-Henonin, L., Schmid, M., Weigel, D., Carter, D.E., Marchand, T., Risseeuw, E., Brogden, D., Zeko, A., Crosby, W.L., Berry, C.C., Ecker, J.R.: Genome-wide insertional mutagenesis of Arabidopsis thaliana. - Science 301: 653-657, 2003. Go to original source...
  2. Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
  3. Aro, E.M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., Battchikova, N., Rintamäki, E.: Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. - J. exp. Bot. 56: 347-356, 2005.
  4. Aro, E.M., Virgin, I., Andersson, B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. - Biochim. biophys. Acta 1143: 113-134, 1993. Go to original source...
  5. Baniwal, S.K., Chan, K.Y., Scharf, K.D., Nover, L.: Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. - J. biol. Chem. 282: 3605-3613, 2007. Go to original source...
  6. Blanvillain, R., Boavida, L.C., McCormick, S., Ow, D.W.: EXPORTIN1 genes are essential for development and function of the gametophytes in Arabidopsis thaliana. - Genetics 180: 1493-1500, 2008. Go to original source...
  7. Clough, S.J., Bent, A.F.: Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. - Plant J. 16: 735-743, 1998. Go to original source...
  8. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V., Schlauch, K., Mittler, R.: Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. - Plant Cell 17: 268-281, 2005a. Go to original source...
  9. Davletova, S., Schlauch, K., Coutu, J., Mittler, R.: The zincfinger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. - Plant Physiol. 139: 847-856, 2005b. Go to original source...
  10. Haasen, D., Köhler, C., Neuhaus, G., Merkle, T.: Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana. - Plant J. 20: 695-705, 1999. Go to original source...
  11. Heerklotz, D., Döring, P., Bonzelius, F., Winkelhaus, S., Nover, L.: The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2. - Mol. Cell. Biol. 21: 1759-1768, 2001. Go to original source...
  12. Hung, S.H., Yu, C.W., Lin, C.H.: Hydrogen peroxide functions as a stress signal in plants. - Bot. Bull. Acad. sin. 46: 1-10, 2005.
  13. Kleinboelting, N., Huep, G., Kloetgen, A., Viehoever, P., Weisshaar, B.: GABI-Kat SimpleSearch: new features of the Arabidopsis thaliana T-DNA mutant database. - Nucl. Acids Res. 40: D1211-D1215, 2012. Go to original source...
  14. Kotak, S., Port, M., Ganguli, A., Bicker, F., Von Koskull-Döring, P.: Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. - Plant J. 39: 98-112, 2004. Go to original source...
  15. Merkle, T.: Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling. - Curr. Genet. 44: 231-260, 2003. Go to original source...
  16. Merkle, T.: Nucleo-cytoplasmic transport of proteins and RNA in plants. - Plant Cell Rep. 30: 153-176, 2011. Go to original source...
  17. Miller, G., Shulaev, V., Mittler, R.: Reactive oxygen signaling and abiotic stress. - Physiol. Plant. 133: 481-489, 2008. Go to original source...
  18. Miller, G., Mittler, R.: Could heat shock transcription factors function as hydrogen peroxide sensors in plants? - Ann. Bot. 98: 279-288, 2006. Go to original source...
  19. Misyura, M., Colasanti, J., Rothstein, S.J.: Physiological and genetic analysis of Arabidopsis thaliana anthocyanin biosynthesis mutants under chronic adverse environmental conditions. - J. exp. Bot. 64: 229-240, 2013. Go to original source...
  20. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue culture. - Physiol. Plant. 15: 473-497, 1962. Go to original source...
  21. Nishiyama, Y., Murata, N.: Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. - Appl. Microbiol. Biotechnol. 98: 8777-8796, 2014. Go to original source...
  22. Niyogi, K.K.: Photoprotection revisited: genetic and molecular approaches. - Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 333-359, 1999. Go to original source...
  23. Nover, L., Bharti, K., Döring, P., Mishra, S.K., Ganguli, A., Scharf, K.D.: Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? - Cell Stress Chaperones 6: 177-189, 2001. Go to original source...
  24. Pérez-Salamó, I., Papdi, C., Rigó, G., Zsigmond, L., Vilela, B., Lumbreras, V., Nagy, I., Horváth, B., Domoki, M., Darula, Z., Medzihradszky, K., Bögre, L., Koncz, C., Szabados, L.: The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. - Plant Physiol. 165: 319-334, 2014. Go to original source...
  25. Personat, J.M., Tejedor-Cano, J., Prieto-Dapena, P., Almoguera, C., Jordano, J.: Co-overexpression of two heat shock factors results in enhanced seed longenity and in synergistic effects on seedling tolerance to severe dehydration and oxidative stress. - BMC Plant Biol. 14: 56, 2014. Go to original source...
  26. Powles, S.B.: Photoinhibition of photosynthesis induced by visible light. - Annu. Rev. Plant Physiol. 35: 15-44, 1984. Go to original source...
  27. Qu, A.L., Ding, Y.F., Jiang, Q., Zhu, C.: Molecular mechanisms of the plant heat stress response. - Biochem. biophys. Res. Commun. 432: 203-207, 2013. Go to original source...
  28. Scarpeci, T.E., Zanor, M.I., Carrillo, N., Mueller-Roeber, B., Valle, E.M.: Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. - Plant mol. Biol. 66: 361-378, 2008a. Go to original source...
  29. Scarpeci, T.E., Zanor, M.I., Valle, E.M.: Investigating the role of plant heat shock proteins during oxidative stress. - Plant Signal. Behav. 3: 856-857, 2008b. Go to original source...
  30. Scharf, K.D., Berberich, T., Ebersberger, I., Nover, L.: The plant heat stress transcription factor (Hsf) family: structure, function and evolution. - Biochim. biophys. Acta 1819: 104-119, 2012. Go to original source...
  31. Scharf, K.D., Heider, H., Höhfeld, I., Lyck, R., Schmidt, E., Nover, L.: The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. - Mol. Cell. Biol. 18: 2240-2251, 1998. Go to original source...
  32. Shim, D., Hwang, J.U., Lee, J., Lee, S., Choi, Y., An, G., Martinoia, E., Lee, Y.: Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. - Plant Cell 21: 4031-4043, 2009. Go to original source...
  33. Takahashi, S., Badger, M.R.: Photoprotection in plants: a new light on photosystem II damage. - Trends Plant Sci. 16: 53-60, 2011. Go to original source...
  34. Takahashi, S., Murata, N.: How do environmental stresses accelerate photoinhibition? - Trends Plant Sci. 13: 178-182, 2008. Go to original source...
  35. Tejedor-Cano, J., Carranco, R., Personat, J.M., Prieto-Dapena, P., Almoguera, C., Espinosa, J.M., Jordano, J.: A passive repression mechanism that hinders synergic transcriptional activation by heat shock factors involved in sunflower seed longevity. - Mol. Plant 7: 256-259, 2014. Go to original source...
  36. Vass, I.: Molecular mechanisms of photodamage in the photosystem II complex. - Biochim. biophys. Acta 1817: 209-217, 2012. Go to original source...
  37. Von Koskull-Döring, P., Scharf, K.D., Nover, L.: The diversity of plant heat stress transcription factors. - Trends Plant Sci. 12: 452-457, 2007. Go to original source...
  38. Wang, L.C., Tsai, M.C., Chang, K.Y., Fan, Y.S., Yeh, C.H., Wu, S.J.: Involvement of the Arabidopsis HIT1/AtVPS53 tethering protein homologue in the acclimation of the plasma membrane to heat stress. - J. exp. Bot. 62: 3609-3620, 2011. Go to original source...
  39. Wang, L.C., Wu, J.R., Chang, W.L., Yeh, C.H., Ke, Y.T., Lu, C.A., Wu, S.J.: Arabidopsis HIT4 encodes a novel chromocentre-localized protein involved in the heat reactivation of transcriptionally silent loci and is essential for heat tolerance in plants. - J. exp. Bot. 64: 1689-1701, 2013. Go to original source...
  40. Wang, L.C., Wu, J.R., Hsu, Y.J., Wu, S.J.: Arabidopsis HIT4, a regulator involved in heat-triggered reorganization of chromatin and release of transcriptional gene silencing, relocates from chromocenters to the nucleoculs in response to heat stress. - New Phytol. 205: 544-554, 2015. Go to original source...
  41. Wu, J.R., Wang, L.C., Lin, Y.R., Weng, C.P., Yeh, C.H., Wu, S.J.: The Arabidopsis heat-intolerant 5 (hit5)/enhanced response to aba 1 (era1) mutant reveals the crucial role of protein farnesylation in plant response to heat stress. - New Phytol. 213: 1181-1193, 2017. Go to original source...
  42. Wu, S.J., Wang, L.C., Yeh, C.H., Lu, C.A., Wu, S.J.: Isolation and characterization of the Arabidopsis heat-intolerant 2 (hit2) mutant reveal the essential role of the nuclear export receptor EXPORTIN1A (XPO1A) in plant heat tolerance. - New Phytol. 186: 833-842, 2010. Go to original source...
  43. Yamanouchi, U., Yano, M., Lin, H., Ashikari, M., Yamada, K.: A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. - Proc. nat. Acad. Sci. USA 99: 7530-7535, 2002. Go to original source...
  44. Yoo, S.D., Cho, Y.H., Sheen, J.: Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. - Nat. Protoc. 2: 1565-1572, 2007. Go to original source...
  45. Zsigmond, L., Szepesi, Á., Tari, I., Rigó, G., Király, A., Szabados, L.: Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis. - Plant Sci. 182: 87-93, 2012. Go to original source...