Abstract
Key message
Transcriptome analysis of barley embryogenic callus from isolated microspore culture under salt stress uncovered a role of translation inhibition and selective activation of stress-specific proteins in cellular defense.
Abstract
Soil salinity is one of the major abiotic stresses which constrains the plant growth and reduces the productivity of field crops. In this study, it was observed that the salt stress in barley isolated microspore culture impacted not only on the quantity of embryogenic callus but also on the quality for later differentiation. The barley microspore-derived embryogenic callus, a transient intermediate form linked cells and plants, was employed for a global transcriptome analysis by RNA sequencing to provide new insights into the cellular adaptation or acclimation to stress. A total of 596 differentially expressed genes (DEGs) were identified, in which 123 DEGs were up-regulated and 473 DEGs were down-regulated in the embryogenic callus produced from microspore culture under salt stress as compared to the control conditions. KEGG pathway analysis identified ‘translation’ (27 DEGs; 12.56 %) as the largest group and followed by ‘folding, sorting and degradation’ (25 DEGs; 11.63 %) in 215 mapped metabolic pathways. The results of RNA-Seq data and quantitative real-time polymerase chain reaction validation showed that the genes related to translation regulation (such as eIF1A, RPLP0, RPLP2, VARS) were down-regulated to control general protein synthesis, and the genes related to endoplasmic reticulum stress response (such as small heat shock protein genes) were selectively up-regulated against protein denaturing during microspore embryogenesis under continuous salt stress. These transcriptional remodeling might affect the essential protein synthesis for the cell development to fulfill totipotency under salt stress.
Similar content being viewed by others
References
Ashraf M, Athar HR, Harris PJC, Kwon TR (2008) Some prospective strategies for improving crop salt tolerance. Adv Agron 97:45–110
Berg M, Rogers R, Muralla R, Meinke D (2005) Requirement of aminoacyl—tRNA synthetases for gametogenesis and embryo development in Arabidopsis. Plant J 44:866–878
Chang F, Wang Y, Wang S, Ma H (2011) Molecular control of microsporogenesis in Arabidopsis. Curr Opin Plant Biol 14:66–73
Chen X, Lin S, Liu Q, Huang J, Zhang W, Lin J, Wang Y, Ke Y, He H (2014) Expression and interaction of small heat shock proteins (sHsps) in rice in response to heat stress. Biochim Biophys Acta 1844:818–828
Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908
Goodall AJ, Kumar P, Tobin AK (2013) Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.). Plant Cell Physiol 54:492–505
Haslbeck M, Vierling E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 427:1537–1548
Hosp J, Tashpulatov A, Roessner U, Barsova E, Katholnigg H, Steinborn R, Melikant B, Lukyanov S, Heberle-Bors E, Touraev A (2007) Transcriptional and metabolic profiles of stress-induced, embryogenic tobacco microspores. Plant Mol Biol 63:137–149
Islam SMS, Tuteja N (2012) Enhancement of androgenesis by abiotic stress and other pretreatments in major crop species. Plant Sci 182:134–144
Jain SM (2001) Tissue culture-derived variation in crop improvement. Euphytica 118:153–166
Lavania D, Dhingra A, Siddiqui MH, Al-Whaibi MH, Grover A (2015) Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant Physiol Biochem 86:100–108
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
Lu R, Wang YF, Sun YF, Shan LL, Chen PD, Huang JH (2008) Improvement of isolated microspore culture of barley (Hordeum vulgare L.): the effect of floret co-culture. Plant Cell Tissue Organ 93:21–27
Maraschin SF, de Priester W, Spaink HP, Wang M (2005) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56:1711–1726
Maraschin SF, Caspers M, Potokina E, Wülfert F, Graner A, Spaink HP, Wang M (2006) cDNA array analysis of stress-induced gene expression in barley androgenesis. Physiol Plantarum 127:535–550
Mayer KF, Waugh R, Brown JW, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, Wise RP, Stein N, International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716
Mohammad AO, Nooshin O, Farajollah SA, Zoran N, Bernd MR (2012) Effect of salt stress on genes encoding translation-associated proteins in Arabidopsis thaliana. Plant Signal Behav 7:1095–1102
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Exp Bot 71:89–98
Rausell A, Kanhonou R, Yenush L, Serrano R, Ros R (2003) The translation initiation factor eIF1A is an important determinant in the tolerance to NaCl stress in yeast and plants. Plant J 34:257–267
Rout G, Senapati S, Panda J (2008) Selection of salt tolerant plants of Nicotiana tabacum L. through in vitro and its biochemical characterization. Acta Biol Hung 59(1):77–92
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124
Ruibal C, Castro A, Carballo V, Szabados L, Vidal S (2013) Recovery from heat, salt and osmotic stress in Physcomitrella patens requires a functional small heat shock protein PpHsp16.4. BMC Plant Biol 13:56–60
Sánchez-Díaz RA, Castillo AM, Vallés MP (2013) Microspore embryogenesis in wheat: new marker genes for early, middle and late stages of embryo development. Plant Reprod 26:287–296
Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genom 10:1–18
Seguí-Simarro JM, Corral-Martínez P, Corredor E, Raska I, Testillano PS, Risueño MC (2011) A change of developmental program induces the remodeling of the interchromatin domain during microspore embryogenesis in Brassica napus L. J Plant Physiol 168:746–757
Shankhdhar D, Shankhdhar SC, Mani RC (2000) In vitro selection for salt tolerance in rice. Biol Plantarum 43:477–480
Shannon MC (1998) Adaptation of plants to salinity. Adv Agron 60:75–119
Soriano M, Li H, Boutilier K (2013) Microspore embryogenesis: establishment of embryo identity and pattern in culture. Plant Reprod 26:181–196
Touraev A, Vicente O, Heberle-Bors E (1997) Initiation of microspore embryogenesis by stress. Trends Plant Sci 2:297–302
Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J 274:1152–1171
Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Biol 42:579–620
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Wang J, Lan P, Gao H, Zheng L, Li W, Schmidt W (2013) Expression changes of ribosomal proteins in phosphate-and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genom 14:783
Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64:391–403
Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620
Zhang JL, Shi HZ (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115:1–22
Zhao C, Shono M, Sun A, Yi S, Li M, Liu J (2007) Constitutive expression of an endoplasmic reticulum small heat shock protein alleviates endoplasmic reticulum stress in transgenic tomato. J Plant Physiol 164:835–841
Acknowledgments
This work was supported by Natural Science Foundation of Shanghai (15ZR1436600) and China Agriculture Research System (CARS-05).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by N. Sreenivasulu.
Rights and permissions
About this article
Cite this article
Liu, Ch., Lu, Rj., Guo, Gm. et al. Transcriptome analysis reveals translational regulation in barley microspore-derived embryogenic callus under salt stress. Plant Cell Rep 35, 1719–1728 (2016). https://doi.org/10.1007/s00299-016-1986-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-016-1986-y