Abstract
Key message
Piriformospora indica symbiosis promoted the growth and photosynthesis, and simultaneously enhanced the resistance against insect herbivory by regulating sporamin-dependent defense in sweet potato.
Abstract
Piriformospora indica (P. indica), a versatile endophytic fungus, promotes the growth and confers resistance against multiple stresses by root colonization in plant hosts. In this study, the effects of P. indica colonization on the growth, physiological change, and herbivore resistance of leaf-vegetable sweet potato cultivar were investigated. P. indica symbiosis significantly improved the biomass in both above- and under-ground parts of sweet potato plants. In comparison with the non-colonized plants, the content of photosynthetic pigments and the efficiency of photosynthesis were increased in P. indica-colonized sweet potato plants. Further investigation showed that the activity of catalase was enhanced in both leaves and roots of sweet potato plants after colonization, but ascorbate peroxidase, peroxidase, and superoxide dismutase were not enhanced. Furthermore, the interaction between P. indica and sweet potato plants also showed the biological function in jasmonic acid (JA)-mediated defense. The plants colonized by P. indica had greatly increased JA accumulation and defense gene expressions, including IbNAC1, IbbHLH3, IbpreproHypSys, and sporamin, leading to elevated trypsin inhibitory activity, which was consistent with a reduced Spodoptera litura performance when larvae fed on the leaves of P. indica-colonized sweet potato plants. The root symbiosis of P. indica is helpful for the plant promoting growth and development and has a strong function as resistance inducers against herbivore attack in sweet potato cultivation by regulating sporamin-dependent defense.







Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- APX:
-
Ascorbate peroxidase
- Car:
-
Carotenoids
- Chl:
-
Chlorophyll
- CAT:
-
Catalase
- ETR:
-
Relative electron transport rate
- P. indica:
-
Piriformospora indica
- JA:
-
Jasmonic acid
- SA:
-
Salicylic acid
- SOD:
-
Superoxide dismutase
- TPI:
-
Trypsin inhibitor
References
Baishya D, Deka P, Kalita MC (2015) In vitro co-cultivation of Piriformospora indica filtrate for improve biomass productivity in Artemisia annua (L.). Symbiosis 66:37–46
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621
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
Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT (2005) Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146:234–243
Chen H-J, Wang S-J, Chen C-C, Yeh K-W (2006) New gene construction strategy in T-DNA vector to enhance expression level of sweet potato sporamin and insect resistance in transgenic Brassica oleracea. Plant Sci 171:367–374
Chen Y-C, Siems WF, Pearce G, Ryan CA (2008) Six peptide wound signals derived from a single precursor protein in Ipomoea batatas leaves activate the expression of the defense gene sporamin. J Biol Chem 283:11469–11476
Chen H-J, Wu S-D, Huang G-J, Shen C-Y, Afiyanti M, Li W-J, Lin Y-H (2012) Expression of a cloned sweet potato catalase SPCAT1 alleviates ethephon-mediated leaf senescence and H2O2 elevation. J Plant Physiol 169:86–97
Chen PJ, Senthilkumar R, Jane WN, He Y, Tian Z, Yeh KW (2014) Transplastomic Nicotiana benthamiana plants expressing multiple defence genes encoding protease inhibitors and chitinase display broad-spectrum resistance against insects, pathogens and abiotic stresses. Plant Biotechnol J 12:503–515
Chen SP, Lin IW, Chen X, Huang YH, Chang SC, Lo HS, Lu HH, Yeh KW (2016a) Sweet potato NAC transcription factor, Ib NAC 1, upregulates sporamin gene expression by binding the SWRE motif against mechanical wounding and herbivore attack. Plant J 86:234–248
Chen S-P, Kuo C-H, Lu H-H, Lo H-S, Yeh K-W (2016b) The sweet potato NAC-domain transcription factor IbNAC1 is dynamically coordinated by the activator IbbHLH3 and the repressor IbbHLH4 to reprogram the defense mechanism against wounding. PLoS Genet 12:e1006397
Chin D-C, Hsieh C-C, Lin H-Y, Yeh K-W (2016) A low glutathione redox state couples with a decreased ascorbate redox ratio to accelerate flowering in Oncidium orchid. Plant and Cell Physiol 57:423–436
Cosme M, Lu J, Erb M, Stout MJ, Franken P, Wurst S (2016) A fungal endophyte helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling. New Phytol 211:1065–1076
de Albuquerque TMR, Sampaio KB, de Souza EL (2019) Sweet potato roots: unrevealing an old food as a source of health promoting bioactive compounds—a review. Trends Food Sci Technol 85:277–286
de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368:270–274
de la Fuente Cantó C, 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. https://doi.org/10.1111/tpj.14781
Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiol 72:297–302
Ghaffari MR, Ghabooli M, Khatabi B, Hajirezaei MR, Schweizer P, Salekdeh GH (2016) Metabolic and transcriptional response of central metabolism affected by root endophytic fungus Piriformospora indica under salinity in barley. Plant Mol Biol 90:699–717
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
Hui F, Liu J, Gao Q, Lou B (2015) Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37:184–191
Hwang S-Y, VanToai TT (1991) Abscisic acid induces anaerobiosis tolerance in corn. Plant Physiol 97:593–597
Iese V, Holland E, Wairiu M, Havea R, Patolo S, Nishi M, Hoponoa T, Bourke RM, Dean A, Waqainabete L (2018) Facing food security risks: the rise and rise of the sweet potato in the Pacific Islands. Global Food Security 18:48–56
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
Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Trop Agric 52:103–122
Kim Y-H, Park S-C, Ji CY, Lee JJ, Jeong JC, Lee H-S, Kwak S-S (2015) Diverse antioxidant enzyme levels in different sweetpotato root types during storage root formation. Plant Growth Regul 75:155–164
Kitayama M, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-um K, Takagaki M, Cha-um S (2020) Calcium and soluble sugar enrichments and physiological adaptation to mild NaCl salt stress in sweet potato (Ipomoea batatas) genotypes. J Horticult Sci Biotechnol. https://doi.org/10.1080/14620316.2020.1749532
Kuo Y-W, Lin J-S, Li Y-C, Jhu M-Y, King Y-C, Jeng S-T (2019) MicroR408 regulates defense response upon wounding in sweet potato. J Exp Bot 70:469–483
Lai Y (2008) Breeding of the new sweet potato variety, Tainung no. 73. J Taiwan Agric. Res 57:279–294
Li YC, Wan WL, Lin JS, Kuo YW, King YC, Chen YC, Jeng ST (2016) Signal transduction and regulation of IbpreproHypSys in sweet potato. Plant, Cell Environ 39:1576–1587
Li D, Mensah RA, Liu F, Tian N, Qi Q, Yeh K, Xuhan X, Cheng C, Lai Z (2019) Effects of Piriformospora indica on rooting and growth of tissue-cultured banana (Musa acuminata cv Tianbaojiao) seedlings. Sci. Horticult 257:108649
Lin H-F, Xiong J, Zhou H-M, Chen C-M, Lin F-Z, Xu X-M, Oelmüller R, Xu W-F, Yeh K-W (2019) Growth promotion and disease resistance induced in Anthurium colonized by the beneficial root endophyte Piriformospora indica. BMC Plant Biol 19:40
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
Long SP, Marshall-Colon A, Zhu X-G (2015) Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 161:56–66
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
Madaan G, Gosal S, Gosal S, Saroa G, Gill M (2013) Effect of microbial inoculants on the growth and yield of micropropagated banana (Musa indica) cv. Grand Naine. J Hortic Sci Biotechnol 88:643–649
Mao L, Lu H, Wang Q, Cai M (2007) Comparative photosynthesis characteristics of Calycanthus chinensis and Chimonanthus praecox. Photosynthetica 45:601–605
Meents AK, Chen S-P, Reichelt M, Lu H-H, Bartram S, Yeh K-W, Mithöfer A (2019) Volatile DMNT systemically induces jasmonate-independent direct anti-herbivore defense in leaves of sweet potato (Ipomoea batatas) plants. Sci Rep 9:1–13
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. Plant J Hortic. https://doi.org/10.1016/j.hpj.2020.01.002
Michal Johnson J, Sherameti I, Ludwig A, Nongbri PL, Sun C, Lou B, Varma A, Oelmüller R (2011) Protocols for Arabidopsis thaliana and Piriformospora indica co-cultivation—A model system to study plant beneficial traits. Endocytobiosis Cell Res 21:101–113
Moreira B, Mendes F, Mendes I, Paula T, Junior PP, Salomão L, Stürmer S, Otoni W, Kasuya M (2015) The interaction between arbuscular mycorrhizal fungi and Piriformospora indica improves the growth and nutrient uptake in micropropagation-derived pineapple plantlets. Sci Hortic 197:183–192
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Pradhan D, Archana M, James G, Chakrabarti S, Vimala B, Naskar S, Sahoo B, Samal S (2015) High starch, beta carotene and anthocyanin rich sweet potato: ascent to future food and nutrition security in coastal and backward areas. Int J Trop Agric 33:397–400
Senthilkumar R, Yeh K-W (2012) Multiple biological functions of sporamin related to stress tolerance in sweet potato (Ipomoea batatas Lam). Biotechnol Adv 30:1309–1317
Šesták Z (1966) Limitations for finding a linear relationship between chlorophyll content and photosynthetic activity. Biol Plant 8:336
Shoukat E, Abideen Z, Ahmed MZ, Gulzar S, Nielsen BL (2019) Changes in growth and photosynthesis linked with intensity and duration of salinity in Phragmites karka. Environ Exp Bot 162:504–514
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
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 2231:606X
Tsai H-J, Shao K-H, Chan M-T, Cheng C-P, Yeh K-W, Oelmüller R, Wang S-J (2020) Piriformospora indica symbiosis improves water stress tolerance of rice through regulating stomata behavior and ROS scavenging systems. Plant Signal Behav 15:1722447
Veronica N, Subrahmanyam D, Kiran TV, Yugandhar P, Bhadana V, Padma V, Jayasree G, Voleti S (2017) Influence of low phosphorus concentration on leaf photosynthetic characteristics and antioxidant response of rice genotypes. Photosynthetica 55:285–293
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Von Wettstein D (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391
Wang S-J, Lan Y-C, Chen S-F, Chen Y-M, Yeh K-W (2002) Wound-response regulation of the sweet potato sporamin gene promoter region. Plant Mol Biol 48:223–231
Wang SQ, Tang J, Hu KD, Huang ZQ, Yang F, Zhang HY, Hu LY, Li YH, Yao GF, Zhang H (2019) Antioxidative system in sweet potato root is activated by low-temperature storage. Sci. Food Agric 99:3824–3833
Wintermans J, De Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biophys Acta 109:448–453
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
Ye W, Jiang J, Lin Y, Yeh K-W, Lai Z, Xu X, Oelmüller R (2019) Colonisation of Oncidium orchid roots by the endophyte Piriformospora indica restricts Erwinia chrysanthemi infection, stimulates accumulation of NBS-LRR resistance gene transcripts and represses their targeting micro-RNAs in leaves. BMC Plant Biol 19:1–16
Yeh K-W, Chen J-C, Lin M-I, Chen Y-M, Lin C-Y (1997) Functional activity of sporamin from sweet potato (Ipomoea batatas Lam.): a tuber storage protein with trypsin inhibitory activity. Plant Mol Biol 33:565–570
Yong B, Wang X, Xu P, Zheng H, Fei X, Hong Z, Ma Q, Miao Y, Yuan X, Jiang Y (2017) Isolation and abiotic stress resistance analyses of a catalase gene from Ipomoea batatas (L.) Lam. Biomed Res Int 2017:2017
Zhong Y, Ahmed S, Deng G, Fan W, Zhang P, Wang H (2019) Improved insect resistance against Spodoptera litura in transgenic sweetpotato by overexpressing Cry1Aa toxin. Plant Cell Rep 38:1439–1448
Acknowledgements
We really thank Prof. Dr. Ralf Oelmüller (Friedrich-Schiller-University Jena) for providing P. indica, Dr. Si-xin Qiu and Dr. Yong-xiang Qiu (Fujian Academy of Agricultural Sciences) for providing sweet potato Fucaishu 18.
Funding
This research was funded by the Fujian Provincial Department of Science and Technology, China (Grant 2017NZ0002-2, 2018N0069 and 2020N0048).
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QL and S-PC conceived and designed the research. QL, Y-WK, K-HL, and WH performed the experiments. QL and CD analyzed the data. K-WY and S-PC wrote the manuscript. All authors have read and agreed to the final version of the manuscript.
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Communicated by Howard S. Judelson.
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Li, Q., Kuo, YW., Lin, KH. et al. Piriformospora indica colonization increases the growth, development, and herbivory resistance of sweet potato (Ipomoea batatas L.). Plant Cell Rep 40, 339–350 (2021). https://doi.org/10.1007/s00299-020-02636-7
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DOI: https://doi.org/10.1007/s00299-020-02636-7