Skip to main content
SpringerLink
Log in

Growth Promotion and Salt-Tolerance Improvement of Gerbera jamesonii by Root Colonization of Piriformospora indica

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Interaction of plants with beneficial microbes is one of the strategies for increasing growth and resistance under environmental stresses. In this study, the effects of a fungus, Piriformospora indica, on growth and salt resistance in gerbera (Gerbera jamesonii L.) seedlings were investigated. After co-cultivation with P. indica, the gerbera roots were colonized by the mature chlamydospores of P. indica. A large increase in plant biomass and enhanced photosynthesis were observed in the P. indica-colonized seedlings. Moreover, these seedlings also exhibited a strong tolerance to salt stress after the colonization. The wilting symptoms, the impairments in chlorophyll, carotenoids, and photosynthesis, and anthocyanin accumulation, that can be caused by salt stress, were alleviated in the P. indica-colonized plants. The malondialdehyde and hydrogen peroxide levels were lower in P. indica-colonized plants than in non-colonized plants under salt treatment, whereas both enzymatic and non-enzymatic antioxidants were not increased by P. indica colonization. Differential expressions of sodium transporter genes and aquaporin genes were found in gerbera plants after P. indica colonization. The P. indica colonization positively regulated the transcription level of genes involved in ionic homeostasis, such as NHX2 and SOS1, while most aquaporin genes were not induced in P. indica-colonized gerbera seedlings exposed to salt stress, except for NIP6;1 gene. These results demonstrate a strategy through plant–microbe interaction to promote Gerbera jamesonii performance under salt stress.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abdelaziz ME, Kim D, Ali S, Fedoroff NV, Al-Babili S (2017) The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na+/K+ homeostasis under salt stress conditions. Int J Exp Plant Biol 263:107

    CAS  Google Scholar 

  • Abdelaziz ME, Abdelsattar M, Abdeldaym EA, Omar MA, Hirt H (2019) Piriformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress. Sci Hortic 256:108532

    Article  CAS  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    Article  CAS  Google Scholar 

  • Baas R, Nijssen HMC, Berg TJMVD, Warmenhoven MG (1995) Yield and quality of carnation (Dianthus caryophyllus L.) and gerbera (Gerbera jamesonii L.) in a closed nutrient system as affected by sodium chloride. Sci Hortic 61:273–284

    Article  Google Scholar 

  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510

    Article  CAS  PubMed  Google Scholar 

  • Carmassi G, Bacci L, Bronzini M, Incrocci L, Maggini R, Bellocchi G, Massa D, Pardossi A (2013) Modelling transpiration of greenhouse gerbera (Gerbera jamesonii H. Bolus) grown in substrate with saline water in a Mediterranean climate. Sci Hortic 156:9–18

    Article  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen J, Zhang H, Zhang X, Tang M (2017) Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Front Plant Sci 8:1739

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen ZH, Lu HH, Hua S, Lin KH, Chen N, Zhang Y, You Z, Kuo YW, Chen SP (2019) Cloning and overexpression of the ascorbate peroxidase gene from the yam (Dioscorea alata) enhances chilling and flood tolerance in transgenic Arabidopsis. J Plant Res 132:857–866

    Article  CAS  PubMed  Google Scholar 

  • de la Fuente CC, Simonin M, King E, Moulin L, Bennett MJ, Castrillo G, Laplaze L (2020) An extended root phenotype: the rhizosphere, its formation and impacts on plant fitness. Plant J 103:951–964

    Article  CAS  Google Scholar 

  • de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368:270–274

    Article  PubMed  CAS  Google Scholar 

  • Deikman J, Philip EH (1995) Induction of anthocyanin accumulation by cytokinins in Arabidopsis thaliana. Plant Physiol 108:47–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Don KKG, Xia YP, Zhu Z, Le C, Wijeratne AW (2010) Some deleterious effects of long-term salt stress on growth, nutrition, and physiology of gerbera (Gerbera jamesonii L.) and potential indicators of its salt tolerance. J Plant Nutr 33:2010–2027

    Article  CAS  Google Scholar 

  • Ghorbani A, Razavi SM, Omran VOG, Pirdashti H (2018) Piriformospora indica inoculation alleviates the adverse effect of NaCl stress on the growth, gas exchange, and chlorophyll fluorescence in tomato (Solanum lycopersicum L.). Plant Biol 20:729–736

    Article  CAS  PubMed  Google Scholar 

  • Ghorbani A, Omran VOG, Razavi SM, Pirdashti H, Ranjbar M (2019) Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Rep 38:1151–1163

    Article  CAS  PubMed  Google Scholar 

  • Gómez Bellot MJ, Carmassi G, Bartalucci M, Sánchez-Blanco MJ, Pardossi A (2018) Growth, evapotranspiration and mineral content of gerbera under combined salinity and excess boron. J Hortic Res 26:61–69

    Article  CAS  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 1:701596

    Google Scholar 

  • Hui F, Liu J, Gao Q, Lou B (2015) Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37:184–191

    Article  CAS  Google Scholar 

  • Hwang SY, VanToai TT (1991) Abscisic acid induces anaerobiosis tolerance in corn. Plant Physiol 97:593–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang W, Pan R, Wu C, Xu L, Abdelaziz ME, Oelmüller R, Zhang W (2020) Piriformospora indica enhances freezing tolerance and post-thaw recovery in Arabidopsis by stimulating the expression of CBF genes. Plant Signal Behav 15:1745472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kadian N, Yadav K, Badda N, Aggarwal A (2013) AM fungi ameliorates growth, yield and nutrient uptake in Cicer arietinum L. under salt stress. Russ Agric Sci 39:321–329

    Article  Google Scholar 

  • Kapilan R, Vaziri M, Zwiazek JJ (2018) Regulation of aquaporins in plants under stress. Biol Res 51:4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Khalid M, Hassani D, Liao J, Xiong X, Bilal M, Huang D (2018) An endosymbiont Piriformospora indica reduces adverse effects of salinity by regulating cation transporter genes, phytohormones, and antioxidants in Brassica campestris ssp. Chinensis. Environ Exp Bot 153:89–99

    Article  CAS  Google Scholar 

  • Lanza M, Rosario Haro R, Conchillo LB, Benito B (2019) The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: fungal ENA ATPases are expressed and regulated at high pH and during plant co-cultivation in salinity. Environ Microbiol 21:3364–3378

    Article  CAS  Google Scholar 

  • Li D, Mensah RA, Liu F, Tian N, Qi Q, Yeh K, Xu X, Cheng C, Lai Z (2019) Effects of Piriformospora indica on rooting and growth of tissue-cultured banana (Musa acuminata cv. Tianbaojiao) seedlings. Sci Hortic 257:108649

    Article  Google Scholar 

  • Lin HF, Xiong J, Zhou HM, Chen CM, Lin FZ, Xu XM, Oelmüller R, Xu WF, Yeh KW (2019) Growth promotion and disease resistance induced in Anthurium colonized by the beneficial root endophyte Piriformospora indica. BMC Plant Boil 19:40

    Article  Google Scholar 

  • Liu H, Senthilkumar R, Ma G, Zou Q, Zhu K, Shen X, Tian D, Hua MS, Oelmüller R, Yeh KW (2019) Piriformospora indica-induced phytohormone changes and root colonization strategies are highly host-specific. Plant Signal Behav 14:1632688

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maathuis FJM, Ahmad I, Patishtan J (2014) Regulation of Na+ fluxes in plants. Front Plant Sci 5:467

    Article  PubMed  PubMed Central  Google Scholar 

  • MacAdam JW, Nelson CJ, Sharp RE (1992) Peroxidase activity in the leaf elongation zone of tall fescue: I spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiol 99:872–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mengistu AA (2020) Endophytes: colonization, behaviour, and their role in defense mechanism. Int J Microbiol 2020:1–8

    Article  CAS  Google Scholar 

  • Mensah RA, Li D, Liu F, Tian N, Sun X, Hao X, Lai Z, Cheng C (2020) Versatile Piriformospora indica and its potential applications in horticultural crops. Hort Plant J 6:55–65

    Google Scholar 

  • Mian AA, Senadheera P, Maathuis FJM (2011) Improving crop salt tolerance: anion and cation transporters as genetic engineering targets. Plant Stress 5:64

    Google Scholar 

  • Munns R, James RA, Luchli AA (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nieves-Cordones M, Lara A, Ródenas R, Amo J, Rivero MR, Martínez V, Rubio F (2019) Modulation of K+ translocation by AKT1 and AtHAK5 in Arabidopsis plants. Plant Cell Environ 42:2357–2371

    Article  CAS  PubMed  Google Scholar 

  • Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26:1–12

    Article  CAS  Google Scholar 

  • Rahman SU, Khalid M, Kayani SI, Tang K (2020) The ameliorative effects of exogenous inoculation of Piriformospora indica on molecular, biochemical and physiological parameters of Artemisia annua L. under arsenic stress condition. Ecotoxicol Environ Saf 206:111202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Rosales MP, Jiang X, Gálvez FJ, Aranda MN, Cubero B, Venema K (2010) Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol 179:366–377

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Charo Azcón RP, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033

    Article  CAS  PubMed  Google Scholar 

  • Sade N, Gebretsadik M, Seligmann R, Schwartz A, Wallach R, Moshelion M (2010) The role of tobacco Aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress. Plant Physiol 152:245–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Šesták Z (1966) Limitations for finding a linear relationship between chlorophyll content and photosynthetic activity. Biol Plant 8:336

    Article  Google Scholar 

  • Sonneveld C, Baas R, Nijssen HMC, de Hoog J (1999) Salt tolerance of flower crops grown in soilless culture. J Plant Nutr 22:1033–1048

    Article  CAS  Google Scholar 

  • Stefanov M, Yotsova E, Rashkov G, Ivanova K, Markovska Y, Apostolova EL (2016) Effects of salinity on the photosynthetic apparatus of two Paulownia lines. Plant Physiol Biochem 101:54–59

    Article  CAS  PubMed  Google Scholar 

  • Su Q, Zheng X, Tian Y, Wang C (2020) Exogenous brassinolide alleviates salt stress in Malus hupehensis Rehd. by regulating the transcription of NHX-type Na+(K+)/H+ antiporters. Front Plant Sci 11:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Sumanta N, Haque CI, Nishika J, Suprakash R (2014) Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Res J Chem Sci 2231:606

    Google Scholar 

  • Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182

    Article  CAS  PubMed  Google Scholar 

  • Tsai HJ, Shao KH, Chan MT, Cheng CP, Yeh KW, Oelmüller R, Wang SJ (2020) Piriformospora indica symbiosis improves water stress tolerance of rice through regulating stomata behavior and ROS scavenging systems. Plant Signal Behav 15:1722447

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vidalie H (2007) Varietal richness and technology for gerbera. PHM Rev Hortic 497:33–41

    Google Scholar 

  • Wintermans J, De Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochim Biophys Acta 109:448–453

    Article  CAS  PubMed  Google Scholar 

  • Wu A, Hammer GL, Doherty A, von Caemmerer S, Farquhar GD (2019) Quantifying impacts of enhancing photosynthesis on crop yield. Nat Plants 5:380–388

    Article  PubMed  Google Scholar 

  • Zhou Y, Diao M, Cui JX, Chen XJ, Liu HY (2018) Exogenous GSH protects tomatoes against salt stress by modulating photosystem II efficiency, absorbed light allocation and H2O2-scavenging system in chloroplasts. J Integr Agric 17:2257–2272

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We really thank Prof. Dr. Kai-Wun Yeh (National Taiwan University) and Prof. Dr. Ralf Oelmüller (Friedrich-Schiller-University Jena) for providing P. indica, and Yunnan Academy of Agricultural Sciences for providing gerbera cv. Yunnanhong.

Funding

This research was funded by the Fujian Provincial Department of Science and Technology, China (Grant 2019N0044, 2019L3025 and 2020S0028).

Author information

Authors and Affiliations

  1. Institute of Flowers, Sanming Academy of Agricultural Sciences, Sanming, Fujian, China

    Weiting Chen, Fazhuang Lin, Changming Chen, Chaoshui Xia, Qiaoling Liao & Yun-Wei Kuo

  2. Department of Horticulture and Biotechnology, Chinese Culture University, Taipei, 11114, Taiwan

    Kuan-Hung Lin

  3. Institute of Dryland Crops, Sanming Academy of Agricultural Sciences, Sanming, Fujian, China

    Shi-Peng Chen

Authors
  1. Weiting Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fazhuang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kuan-Hung Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Changming Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chaoshui Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qiaoling Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shi-Peng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yun-Wei Kuo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SPC and YWK conceived and designed the experiments; WC, FL, KHL, CC, CX, QL, and YWK performed the experiments and analyzed the data; SPC and YWK wrote and revise the paper. All authors approved the final manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Shi-Peng Chen or Yun-Wei Kuo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Rhonda Peavy.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 642 kb)

Supplementary file2 (PDF 90 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, W., Lin, F., Lin, KH. et al. Growth Promotion and Salt-Tolerance Improvement of Gerbera jamesonii by Root Colonization of Piriformospora indica. J Plant Growth Regul 41, 1219–1228 (2022). https://doi.org/10.1007/s00344-021-10385-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10385-4

Keywords

Search

Navigation