Skip to main content
Log in

A novel inhibitor of cytokinin degradation (INCYDE) influences the biochemical parameters and photosynthetic apparatus in NaCl-stressed tomato plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The effect of 2-chloro-6-(3-methoxyphenyl)aminopurine [inhibitor of cytokinin degradation (INCYDE)] at 10 nM on growth, biochemical and photosynthetic efficiency in sodium chloride (NaCl)-stressed (75, 100 and 150 mM) tomato plants was investigated. NaCl-induced decline in plant vigor index was slightly reversed by both drenching and foliar application of INCYDE. Foliar application of INCYDE significantly increased the flower number in the control and 75 mM NaCl-supplemented plants, while drenching was more effective in 150 mM NaCl-stressed plants. Antioxidant enzymes (peroxidase, catalase and superoxide dismutase) were enhanced in the presence of INCYDE in the control and NaCl-stressed plants. Higher concentration of malondialdehyde (MDA) associated with oxidative (lipid peroxidation) damage in leaf tissue which was evident in the presence of NaCl stress was significantly attenuated with the drenching and foliar application of INCYDE. Regardless of NaCl concentration, application of INCYDE had no significant influence on maximum quantum efficiency of photosystem II. However, the reduced quantum yield of photosystem II and coefficient of photochemical quenching under continuous illumination with actinic light at four intensities (264, 488, 800 and 1,200 µmol m−2 s−1) in NaCl-stressed (100 and 150 mM) tomato plants were significantly alleviated by drenching application with INCYDE. Non-photochemical quenching of the singlet excited state of chlorophyll a and relative electron transfer rate were generally higher in INCYDE-treated plants than in the controls. From an agricultural perspective, these findings indicate the potential of INCYDE in protecting plants against NaCl stress and the possibility of enhanced productivity.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

CAT:

Catalase

CK:

Cytokinin

CKX:

Cytokinin oxidase/dehydrogenase

DW:

Dry weight

ETR:

Relative electron transport rate

Fm:

Maximum fluorescence yield

Fo:

Minimum fluorescence yield

Fv:

Variable fluorescence (Fm–Fo)

Fv/Fm:

Maximum quantum efficiency of PSII

FW:

Fresh weight

GAE:

Gallic acid equivalents

HS:

Hoagland’s nutrient solution

INCYDE:

Inhibitor of cytokinin degradation 2-chloro-6-(3-methoxyphenyl)aminopurine

MDA:

Malondialdehyde

NaCl:

Sodium chloride

NPQ:

Non-photochemical quenching

PAR:

Photosynthetically available radiation

POD:

Peroxidase

ϕPSII :

Actual quantum yield of photosystem II

PSII:

Photosystem II

PVI:

Plant vigor index

qP:

Photochemical quenching

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

References

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  PubMed  CAS  Google Scholar 

  • Amoo SO, Aremu AO, Moyo M, Szüčová L, Doležal K, Van Staden J (2014) Physiological effects of a novel aromatic cytokinin analogue in micropropagated Aloe arborescens and Harpagophytum procumbens. Plant Cell Tiss Organ Cult 116:17–26

    Article  CAS  Google Scholar 

  • Aremu AO, Bairu MW, Novák O, Plačková L, Zatloukal M, Doležal K, Finnie JF, Strnad M, Van Staden J (2012a) Physiological responses and endogenous cytokinin profiles of tissue-cultured ‘Williams’ bananas in relation to roscovitine and an inhibitor of cytokinin oxidase/dehydrogenase (INCYDE) treatments. Planta 236:1775–1790

    Article  PubMed  CAS  Google Scholar 

  • Aremu AO, Bairu MW, Szüčová L, Finnie JF, Van Staden J (2012b) The role of meta-topolins on the photosynthetic pigment profiles and foliar structures of micropropagated ‘Williams’ bananas. J Plant Physiol 169:1530–1541

    Article  PubMed  CAS  Google Scholar 

  • Arthur GD, Aremu AO, Kulkarni MG, Van Staden J (2012) Vermicompost leachate alleviates deficiency of phosphorus and potassium in tomato seedlings. HortScience 47:1304–1307

    Google Scholar 

  • Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745

    Article  PubMed  CAS  Google Scholar 

  • Auer CA (1997) Cytokinin conjugation: recent advances and patterns in plant evolution. Plant Growth Regul 23:17–32

    Article  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  PubMed  CAS  Google Scholar 

  • Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23:69–80

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Beckett RP, Marschall M, Laufer Z (2005) Hardening enhances photoprotection in the moss Atrichum androgynum during rehydration by increasing fast-rather than slow-relaxing quenching. J Bryol 27:7–12

    Article  Google Scholar 

  • Bergougnoux V (2014) The history of tomato: from domestication to biopharming. Biotechnol Adv 32:170–189

    Article  PubMed  CAS  Google Scholar 

  • Bernier G (2013) My favourite flowering image: the role of cytokinin as a flowering signal. J Exp Bot 64:5795–5799

    Article  PubMed  CAS  Google Scholar 

  • Bilyeu KD, Cole JL, Laskey JG, Riekhof WR, Esparza TJ, Kramer MD, Morris RO (2001) Molecular and biochemical characterization of a cytokinin oxidase from maize. Plant Physiol 125:378–386

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504

    Article  PubMed  Google Scholar 

  • Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70

    Article  PubMed  CAS  Google Scholar 

  • Chaudhury AM, Letham S, Craig S, Dennis ES (1993) amp1—a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J 4:907–916

    Article  CAS  Google Scholar 

  • Chernyad’ev II (2009) The protective action of cytokinins on the photosynthetic machinery and productivity of plants under stress (review). Appl Biochem Microbiol 45:351–362

    Article  Google Scholar 

  • Chinsamy M, Kulkarni MG, Van Staden J (2013) Garden-waste-vermicompost leachate alleviates salinity stress in tomato seedlings by mobilizing salt tolerance mechanisms. Plant Growth Regul 71:41–47

    Article  CAS  Google Scholar 

  • Cuartero J, Fernández-Muñoz R (1998) Tomato and salinity. Sci Hortic 78:83–125

    Article  Google Scholar 

  • D’Aloia M, Bonhomme D, Bouché F, Tamseddak K, Ormenese S, Torti S, Coupland G, Périlleux C (2011) Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 65:972–979

    Article  PubMed  Google Scholar 

  • Fan M, Bie Z, Krumbein A, Schwarz D (2011) Salinity stress in tomatoes can be alleviated by grafting and potassium depending on the rootstock and K-concentration employed. Sci Hortic 130:615–623

    Article  CAS  Google Scholar 

  • Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452

    Article  PubMed  Google Scholar 

  • Gálvez FJ, Baghour M, Hao G, Cagnac O, Rodríguez-Rosales MP, Venema K (2012) Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species. Plant Physiol Biochem 51:109–115

    Article  PubMed  Google Scholar 

  • Gemrotová M, Kulkarni MG, Stirk WA, Strnad M, Van Staden J, Spíchal L (2013) Seedlings of medicinal plants treated with either a cytokinin antagonist (PI-55) or an inhibitor of cytokinin degradation (INCYDE) are protected against the negative effects of cadmium. Plant Growth Regul 71:137–145

    Article  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179

    Article  PubMed  CAS  Google Scholar 

  • He Z, He C, Zhang Z, Zou Z, Wang H (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B Biointerf 59:128–133

    Article  CAS  Google Scholar 

  • Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès J, Al-Juburi HJ, Chang-Xing Z, Hong-Bo S, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436

    Article  Google Scholar 

  • Katerji N, van Hoorn JW, Hamdy A, Mastrorilli M (2000) Salt tolerance classification of crops according to soil salinity and to water stress day index. Agr Wat Manag 43:99–109

    Article  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  PubMed  CAS  Google Scholar 

  • Landi M, Remorini D, Pardossi A, Guidi L (2013) Boron excess affects photosynthesis and antioxidant apparatus of greenhouse Cucurbita pepo and Cucumis sativus. J Plant Res 126:775–786

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Douce R, Packer L (eds) Methods in enzymology, vol 148., Academic PressNew York, USA, pp 350–382

    Google Scholar 

  • Lu S-w, Li T-l, Jiang J (2009) Tomato key sucrose metabolizing enzyme activities and gene expression under NaCl and PEG iso-osmotic stresses. Agr Sci China 8:1046–1052

    Article  CAS  Google Scholar 

  • Martins N, Osório ML, Gonçalves S, Osório J, Palma T, Romano A (2013) Physiological responses of Plantago algarbiensis and P. almogravensis shoots and plantlets to low pH and aluminum stress. Acta Physiol Plant 35:615–625

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Mrízová K, Jiskrová E, Vyroubalová Š, Novák O, Ohnoutková L, Pospíšilová H, Frébort I, Harwood WA, Galuszka P (2013) Overexpression of cytokinin dehydrogenase genes in Barley (Hordeum vulgare cv. Golden Promise) fundamentally affects morphology and fertility. PLoS ONE 8:e79029

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakaune M, Hanada A, Yin Y-G, Matsukura C, Yamaguchi S, Ezura H (2012) Molecular and physiological dissection of enhanced seed germination using short-term low-concentration salt seed priming in tomato. Plant Physiol Biochem 52:28–37

    Article  PubMed  CAS  Google Scholar 

  • Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    Article  PubMed  CAS  Google Scholar 

  • Prokopová J, Špundová M, Sedlářová M, Husičková A, Novotný R, Doležal K, Nauš J, Lebeda A (2010) Photosynthetic responses of lettuce to downy mildew infection and cytokinin treatment. Plant Physiol Biochem 48:716–723

    Article  PubMed  Google Scholar 

  • Rady MM (2012) A novel organo-mineral fertilizer can mitigate salinity stress effects for tomato production on reclaimed saline soil. S Afr J Bot 81:8–14

    Article  CAS  Google Scholar 

  • Reusche M, Klásková J, Thole K, Truskina J, Novák O, Janz D, Strnad M, Spíchal L, Lipka V, Teichmann T (2013) Stabilization of cytokinin levels enhances Arabidopsis resistance gainst Verticillium longisporum. Mol Plant Microb Interact 26:850–860

    Article  CAS  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    Article  PubMed  CAS  Google Scholar 

  • Schmülling T, Werner T, Riefler M, Krupková E, Bartrina y Manns I (2003) Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J Plant Res 116:241–252

    Article  PubMed  Google Scholar 

  • Schnablová R, Synková H, Vicánková A, Burketová L, Eder J, Cvikrová M (2006) Transgenic ipt tobacco overproducing cytokinins overaccumulates phenolic compounds during in vitro growth. Plant Physiol Biochem 44:526–534

    Article  PubMed  Google Scholar 

  • Shi X, Gupta S, Lindquist IE, Cameron CT, Mudge J, Rashotte AM (2013) Transcriptome analysis of cytokinin response in tomato leaves. PLoS ONE 8:e55090

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Šmehilová M, Spíchal L (2014) The biotechnological potential of cytokinin status manipulation. In: Nick P, Opatrny Z (eds) Applied plant cell biology. Springer, Berlin Heidelberg, pp 103–130

    Chapter  Google Scholar 

  • Sunmonu TO, Van Staden J (2014) Phytotoxicity evaluation of six fast-growing tree species in South Africa. S Afr J Bot 90:101–106

    Article  CAS  Google Scholar 

  • Tamagnone L, Merida A, Stacey N, Plaskitt K, Parr A, Chang C-F, Lynn D, Dow JM, Roberts K, Martin C (1998) Inhibition of phenolic acid metabolism results in precocious cell death and altered cell morphology in leaves of transgenic tobacco plants. Plant Cell 10:1801–1816

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255

    Article  PubMed  CAS  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20

    Article  PubMed  CAS  Google Scholar 

  • Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538

    Article  PubMed  CAS  Google Scholar 

  • Zalabák D, Pospíšilová H, Šmehilová M, Mrízová K, Frébort I, Galuszka P (2013) Genetic engineering of cytokinin metabolism: prospective way to improve agricultural traits of crop plants. Biotechnol Adv 31:97–117

    Article  PubMed  Google Scholar 

  • Zalabák D, Galuszka P, Mrízová K, Podlešáková K, Gu R, Frébortová J (2014) Biochemical characterization of the maize cytokinin dehydrogenase family and cytokinin profiling in developing maize plantlets in relation to the expression of cytokinin dehydrogenase genes. Plant Physiol Biochem 74:283–293

    Article  PubMed  Google Scholar 

  • Zatloukal M, Gemrotová M, Dolezal K, Havlícek L, Spíchal L, Strnad M (2008) Novel potent inhibitors of A. thaliana cytokinin oxidase/dehydrogenase. Bioorg Med Chem 16:9268–9275

    Article  PubMed  CAS  Google Scholar 

  • Zhang R, Li J, Guo S, Tezuka T (2009) Effects of exogenous putrescine on gas-exchange characteristics and chlorophyll fluorescence of NaCl-stressed cucumber seedlings. Photosynth Res 100:155–162

    Article  PubMed  CAS  Google Scholar 

  • Zribi L, Fatma G, Fatma R, Salwa R, Hassan N, Néjib RM (2009) Application of chlorophyll fluorescence for the diagnosis of salt stress in tomato “Solanum lycopersicum (variety Rio Grande)”. Sci Hortic 120:367–372

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The Claude Leon Foundation (AOA), National Research Foundation (NAM) and University of KwaZulu-Natal (MGK and TOS), South Africa are thanked for financial support. MZ, LS and KD were supported by the Ministry of Education, Youth and Sports, Czech Republic (Grant L01204 from the National Program of Sustainability) as well as by IGA of Palacký University (Grant IGA_PrF_2014006). KD and LS also acknowledges the support of the Operational Program Education for Competitiveness—European Social Fund (project CZ.1.07/2.3.00/20.0165). We sincerely thank Prof R.P. Beckett for his assistance with chlorophyll fluorescence experiments as well as Mrs Alison Young (UKZN Botanical Garden, Pietermaritzburg, South Africa) and her staff for maintaining the greenhouse facilities. We sincerely thank the two anonymous reviewers for their critical and constructive suggestions.

Conflict of interest

We declare that there are no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johannes Van Staden.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aremu, A.O., Masondo, N.A., Sunmonu, T.O. et al. A novel inhibitor of cytokinin degradation (INCYDE) influences the biochemical parameters and photosynthetic apparatus in NaCl-stressed tomato plants. Planta 240, 877–889 (2014). https://doi.org/10.1007/s00425-014-2126-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-014-2126-y

Keywords

Navigation