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Environmental stress alters genes expression and induces ovule abortion: reactive oxygen species appear as ovules commit to abort

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Abstract

Environmental stress dramatically reduces plant reproduction. Previous results showed that placing roots in 200 mM NaCl for 12 h caused 90% of the developing Arabidopsis ovules to abort (Sun et al. in Plant Physiol 135:2358–2367, 2004). To discover the molecular responses that occur during ovule abortion, gene expression was monitored using Affymetrix 24k genome arrays. Transcript levels were measured in pistils that were stressed for 6, 12, 18, and 24 h, then compared with the levels in healthy pistils. Over the course of this experiment, a total of 535 salt-responsive genes were identified. Cluster analysis showed that differentially expressed genes exhibited reproducible changes in expression. The expression of 65 transcription factors, some of which are known to be involved in stress responses, were modulated during ovule abortion. In flowers, salt stress led to a 30-fold increase in Na+ ions and modest, but significant, decreases in the accumulation of other ions. The expression of cation exchangers and ion transporters were induced, presumably to reestablish ion homeostasis following salt stress. Genes that encode enzymes that detoxify reactive oxygen species (ROS), including ascorbate peroxidase and peroxidase, were downregulated after ovules committed to abort. These changes in gene expression coincided with the synthesis of ROS in female gametophytes. One day after salt stress, ROS spread from the gametophytes to the maternal chalaza and integuments. In addition, genes encoding proteins that regulate ethylene responses, including ethylene biosynthesis, ethylene signal transduction and ethylene-responsive transcription factors, were upregulated after stress. Hypotheses are proposed on the basis of this expression analysis, which will be evaluated further in future experiments.

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Abbreviations

aRNA:

Antisense RNA

CH2DCFDA:

5-(and −6)-carboxy-2′,7′-dichlorodihydro-fluorescein diacetate

DChip:

DNA-chip analyzer

DREB:

Dehydration-responsive element-binding

ERF:

Ethylene response factor

LCB:

Lower confidence bound

MAS:

Affymetrix microarray suite

PCD:

Programmed cell death

ROS:

Reactive oxygen species

References

  • Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  PubMed  CAS  Google Scholar 

  • Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplast: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  PubMed  CAS  Google Scholar 

  • Asch F, Dingkuhn M, Wittstock C, Doerffling K (1999) Sodium and potassium uptake of rice panicles as affected by salinity and season in relation to yield and yield components. Plant Soil 207:133–145

    Article  Google Scholar 

  • Bohnert HJ, Ayoubi P, Borchert C, Bressan RA, Burnap RL, Cushman JC, Cushman MA, Deyholos M, Fischer R, Galbraith DW (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39:295–311

    Article  CAS  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Response to abiotic stress. In: Jones R (ed) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1158–1203

    Google Scholar 

  • Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang H-S, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA and others (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574

    Article  PubMed  CAS  Google Scholar 

  • Dat J, Vandenabeele S, Vranová E, Montagu MV, Inzé D, Breusegem FV (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, A-H-Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172

    Article  PubMed  CAS  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • Ermolaeva O, Rastogi M, Pruitt KD, Schuler GD, Bittner ML, Chen Y, Simon R, Meltzer P, Trent JM, Boguski MS (1998) Data management and analysis for gene expression arrays. Nat Genet 20:19–23

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Q Rev Biol 61:313–337

    Article  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    Article  PubMed  CAS  Google Scholar 

  • Gao D, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004) Self-reporting Arabidopsis expressing pH and Ca2+ indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134:898–908

    Article  PubMed  CAS  Google Scholar 

  • Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

    Article  Google Scholar 

  • Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular response to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • He CJ, Morgan PW, Drew MC (1996) Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol 112:463–472

    PubMed  CAS  Google Scholar 

  • Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122

    Article  PubMed  CAS  Google Scholar 

  • Huang S, An YQ, McDowell JM, McKinney EC, Meagher RB (1997) The Arabidopsis ACT11 actin gene is strongly expressed in tissues of the emerging inflorescence, pollen, and developing ovules. Plant Mol Biol 33:125–139

    Article  PubMed  CAS  Google Scholar 

  • John I, Hackett R, Cooper W, Drake R, Farrell A, Grierson D (1997) Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol Biol 33:641–651

    Article  PubMed  CAS  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotech 17:287–291

    Article  CAS  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–906

    Article  PubMed  CAS  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P and others (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855

    Article  PubMed  CAS  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Article  PubMed  CAS  Google Scholar 

  • Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681–687

    Article  PubMed  CAS  Google Scholar 

  • Krause G (1994) The role of oxygen in photoinhibition of the photosynthesis. In: Mullineaux P (eds) Cause of photooxidative stress and amelioration of defense system in plants. CRC, Boca Raton

    Google Scholar 

  • Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  PubMed  CAS  Google Scholar 

  • Kuk YI, Shin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43:2109–2117

    Article  CAS  Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853

    Article  PubMed  CAS  Google Scholar 

  • Li C, Wong WH (2001a) Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31–36

    Article  PubMed  CAS  Google Scholar 

  • Li C, Wong WH (2001b) Model-based analysis of oligonucleotide arrays: Model validation, design issues and standard error application. Genome Biol 2:0032.1–0032.11

    Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  CAS  Google Scholar 

  • Lloyd DG (1980) Sexual strategies in plants I. A hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytol 86:69–79

    Article  Google Scholar 

  • Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993

    Article  PubMed  CAS  Google Scholar 

  • Mergemann H, Sauter M (2000) Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 124:609–614

    Article  PubMed  CAS  Google Scholar 

  • Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjarvi J (2002) Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol 130:1918–1926

    Article  PubMed  CAS  Google Scholar 

  • Munne-Bosch S, Penuelas J, Asensio D, Llusia J (2004) Airborne ethylene may alter antioxidant protection and reduce tolerance of holm oak to heat and drought stress. Plant Physiol 136:2937–2947

    Article  PubMed  CAS  Google Scholar 

  • Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742

    PubMed  CAS  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    Article  PubMed  CAS  Google Scholar 

  • Quesada V, Garcia-Martinez S, Piqueras P, Ponce MR, Micol JL (2002) Genetic architecture of NaCl tolerance in Arabidopsis. Plant Physiol 130:951–963

    Article  PubMed  CAS  Google Scholar 

  • Raes D, Deckers J, Diallo M (1995) Water requirements for salt control in rice schemes in the Senegal river delta and valley. Irrig Drain Syst 9:129–141

    Article  Google Scholar 

  • Rao MV, Lee H-i, Davis KR (2002) Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J 32:447–456

    Article  PubMed  CAS  Google Scholar 

  • Rus A, Lee B-h, Munoz-Mayor A, Sharkhuu A, Miura K, Zhu J-K, Bressan RA, Hasegawa PM (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol 136:2500–2511

    Article  PubMed  CAS  Google Scholar 

  • Sablowski RWM, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103

    Article  PubMed  CAS  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  PubMed  CAS  Google Scholar 

  • Santos CLV, Campos A, Azevedo H, Caldeira G (2001) In situ and in vitro senescence induced by KCl stress: nutritional imbalance, lipid peroxidation and antioxidant metabolism. J Exp Bot 52:351–360

    Article  PubMed  CAS  Google Scholar 

  • Schadt EE, Li C, Ellis B, Wong WH (2001) Feature extraction and normalization algorithms for high-density oligonucleotide gene expression array data. J Cell Biochem Suppl 37:120–125

    Article  PubMed  CAS  Google Scholar 

  • Schneitz K, Hulskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7:731–749

    Article  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu J-K (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  PubMed  CAS  Google Scholar 

  • Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  PubMed  CAS  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  PubMed  CAS  Google Scholar 

  • Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482

    Article  PubMed  CAS  Google Scholar 

  • Stephenson A (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279

    Article  Google Scholar 

  • Stephenson A (1992) The regulation of maternal investment in plants. In: Grace J (eds) Fruit and seed production: aspects of development, environmental physiology and ecology. Cambridge University Press, New York, pp 151–171

    Google Scholar 

  • Su H, Golldack D, Zhao C, Bohnert HJ (2002) The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol 129:1482–1493

    Article  PubMed  CAS  Google Scholar 

  • Sun K, Hunt K, Hauser BA (2004) Ovule abortion in Arabidopsis triggered by stress. Plant Physiol 135:2358–2367

    Article  PubMed  CAS  Google Scholar 

  • Tran L-SP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress. Plant Cell 16:2481–2498

    Article  PubMed  CAS  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg E and others (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185

    Article  PubMed  CAS  Google Scholar 

  • Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel H-J, Overmyer K, Kangasjarvi J, Sandermann H, Langebartels C (2002) Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ 25:717–726

    Article  CAS  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua N-H (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  PubMed  CAS  Google Scholar 

  • Zhang H-X, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotech 19:765–768

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Mick Popp and others in the UF ICBR microarray facility for their attention to detail, which allowed us to collect an accurate, reproducible microarray hybridization data. In addition, we thank Michelle Mack and Jennie DeMarco for their assistance with elemental analysis. This research was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service (grant# 2002-35100-12109) and a UF Alumni Fellowship (Kelian Sun).

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  1. Department of Botany, University of Florida, Gainesville, FL, 32611-8526, USA

    Kelian Sun & Bernard A. Hauser

  2. Department of Statistics, University of Florida, Gainesville, FL, 32611-8545, USA

    Yuehua Cui

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  1. Kelian Sun
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Correspondence to Bernard A. Hauser.

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Sun, K., Cui, Y. & Hauser, B.A. Environmental stress alters genes expression and induces ovule abortion: reactive oxygen species appear as ovules commit to abort. Planta 222, 632–642 (2005). https://doi.org/10.1007/s00425-005-0010-5

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