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Paper-based electroanalytical devices for in situ determination of free 3-indoleacetic acid and salicylic acid in living Pyropia haitanensis thallus under various environmental stresses

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Abstract

Phytohormones play a vital role in regulating plant developmental processes and signaling for defense, but little is known of the specific functions of phytohormones in Pyropia haitanensis. In this study, paper-based electroanalytical devices for sensitive, in situ detection of free 3-indoleacetic acid (IAA) and salicylic acid (SA) based on their electrocatalytic oxidation under differential pulse voltammetry in P. haitanensis thallus were built. Then, this method was used to detect free IAA and SA in P. haitanensis thallus under different environmental stresses, including high temperature, high irradiance, desiccation, and exposure to ultraviolet radiation. The concentrations of SA increased after the different environmental stresses were imposed, while the concentrations of IAA significantly decreased after desiccation, exposure to ultraviolet radiation and high light. During exposure to high temperature, the concentrations of IAA increased in the first hour after treatment, and then returned to the normal level for the following 5 h. All of the electrocatalytic measurements were supported by measuring expression levels of IAA and SA synthesis-related genes in P. haitanensis. These results help to systematically clarify that IAA acts as a negative regulatory factor in regulating plant resistance to environmental stresses except for high temperature, while SA plays the opposite role.

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References

  • Amin SA, Hmelo LR, Van Tol HM, Durham BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101

    CAS  PubMed  Google Scholar 

  • Bai Y, Du F, Liu H (2010) Determination strategies of phytohormones: recent advances. Anal Methods 2:1867–1873

    CAS  Google Scholar 

  • Bandurska H, Cieślak M (2013) The interactive effect of water deficit and UV-B radiation on salicylic acid accumulation in barley roots and leaves. Environ Exp Bot 94:9–18

    CAS  Google Scholar 

  • Bradley PM (1991) Plant hormones do have a role in controlling growth and development of algae. J Phycol 27:317–321

    CAS  Google Scholar 

  • Cao J, Wang J, Wang S, Xu X (2016) Porphyra species: a mini-review of its pharmacological and nutritional properties. J Med Food 19:111–119

    CAS  PubMed  Google Scholar 

  • Chen J, Chen Y, Yang R, Luo Q, Chen H, Xu J, Yan X, Shen B (2018) Response to wound-activated stress through a lipid oxidative metabolic pathway in Pyropia haitanensis. Algal Res 35:206–214

    Google Scholar 

  • Chen H, Yang R, Chen J, Luo Q, Cui X, Yan X, Gerwick WH (2019) 1-Octen-3-ol, a self-stimulating oxylipin messenger, can prime and induce defense of marine alga. BMC Plant Biol 19:37

    PubMed  PubMed Central  Google Scholar 

  • de Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plantarum 147:296–306

    Google Scholar 

  • Du F, Ruan G, Liu H (2012) Analytical methods for tracing plant hormones. Anal Bioanal Chem 403:55–74

    CAS  PubMed  Google Scholar 

  • Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397

    PubMed  PubMed Central  Google Scholar 

  • Enders TA, Strader LC (2015) Auxin activity: past, present, and future. Am J Bot 102:180–196

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu L, Hamzeh M, Dodard S, Zhao YH, Sunahara GI (2015) Effects of TiO2 nanoparticles on ROS production and growth inhibition using freshwater green algae pre-exposed to UV irradiation. Environ Toxicol Phar 39:1074–1080

    CAS  Google Scholar 

  • Hou S, Zou T, Wang F, Sun X, Xu N (2017) Effects of methyl jasmonate and salicylic acid on the growth and stress resistance of Pyropia haitanensis. Mar Sci 1:104–112

    Google Scholar 

  • Janda M, Ruelland E (2015) Magical mystery tour: salicylic acid signalling. Environ Exp Bot 114:117–128

    CAS  Google Scholar 

  • Kumar M, Gupta V, Trivedi N, Kumari P, Bijo AJ, Reddy CR, Jha B (2011) Desiccation induced oxidative stress and its biochemical responses in intertidal red alga Gracilaria corticata (Gracilariales, Rhodophyta). Environ Exp Bot 72:194–201

    CAS  Google Scholar 

  • Lankelma J, Nie Z, Carrilho E, Whitesides GM (2012) Based analytical device for electrochemical flow-injection analysis of glucose in urine. Anal Chem 84:4147–4152

    CAS  PubMed  Google Scholar 

  • Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock JM, Ljung K, Charrier B (2010) Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol 153:128–144

    PubMed  PubMed Central  Google Scholar 

  • Liu JT, Hu LS, Liu YL, Chen RS, Cheng Z, Chen SJ, Amatore C, Huang WH, Huo KF (2014) Real-time monitoring of auxin vesicular exocytotic efflux from single plant protoplasts by amperometry at microelectrodes decorated with nanowires. Angew Chem Int Edn 53:2643–2647

    CAS  Google Scholar 

  • Li X, He P, Xu J, Fu G, Chen Y (2017) Effect of nitrogen and phosphorus on the growth and amino acid contents of Porphyra yezoensis. Aquac Res 48:2798–2802

    CAS  Google Scholar 

  • Li X, Yang R, Gong Y, Chen H (2018) The Arabidopsis mediator complex subunit MED19a is involved in ABI5-mediated ABA responses. J Plant Biol 61:97–110

    CAS  Google Scholar 

  • Matsuura T, Mori IC, Ikeda Y, Hirayama T, Mikami K (2018) Comprehensive phytohormone quantification in the red alga Pyropia yezoensis by liquid chromatography–mass spectrometry. In: Charrier B, Wichard T, Reddy CRK (eds) Protocols for macroalgae research. CRC Press, Boca Raton, pp 225–236

    Google Scholar 

  • McLamore ES, Diggs A, Calvo Marzal P, Shi J, Blakeslee JJ, Peer WA, Murphy AS, Porterfield DM (2010) Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. Plant J 63:1004–1016

    CAS  PubMed  Google Scholar 

  • Mikami K, Mori IC, Matsuura T, Ikeda Y, Kojima M, Sakakibara H, Hirayama T (2016) Comprehensive quantification and genome survey reveal the presence of novel phytohormone action modes in red seaweeds. J Appl Phycol 28:2539–2548

    Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A, Talarek M, Bralska M, Zambrzycka E (2015) The effect of lead on the growth, content of primary metabolites, and antioxidant response of green alga Acutodesmus obliquus (Chlorophyceae). Environ Sci Pollut Res 22:19112–19123

    CAS  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka-Szelewa E, Bralska M (2018) Exogenously applied auxins and cytokinins ameliorate lead toxicity by inducing antioxidant defence system in green alga Acutodesmus obliquus. Plant Physiol Bioch 132:535–546

    CAS  Google Scholar 

  • Qian F, Luo Q, Yang R, Zhu Z, Chen H, Yan X (2015) The littoral red alga Pyropia haitanensis uses rapid accumulation of floridoside as the desiccation acclimation strategy. J Appl Phycol 27:621–632

    CAS  Google Scholar 

  • Seo H, Kriechbaumer V, Park WJ (2016) Modern quantitative analytical tools and biosensors for functional studies of auxin. J Plant Biol 59:93–104

    CAS  Google Scholar 

  • Song Y, Cui XS, Chen JJ, Yang R, YAN X (2017) The profiling of eleven phytohormones in Pyropia haitanensis under different high-temperature environments. J Fisheries China 41:1578–1587

    Google Scholar 

  • Stirk WA, Van Staden J (2014) Plant growth regulators in seaweeds: occurrence, regulation and functions. In: Bourgougnon N (ed) Sea plants. Academic Press, Waltham, pp 125–153

    Google Scholar 

  • Sun LJ, Zhou JJ, Pan JL, Liang YY, Fang ZJ, Xie Y, Yang H, Gu HY, Bao N (2018) Electrochemical mapping of indole-3-acetic acid and salicylic acid in whole pea seedlings under normal conditions and salinity. Sensor Actuat B 276:545–551

    CAS  Google Scholar 

  • Sun M, Johnson MA (2015) Measurement of total antioxidant capacity in sub-μL blood samples using craft paper-based analytical devices. RSC Adv 5:55633–55639

    CAS  PubMed  Google Scholar 

  • Suh SS, Oh SK, Lee SG, Kim IC, Kim S (2017) Porphyra-334, a mycosporine-like amino acid, attenuates UV-induced apoptosis in HaCaT cells. Acta Pharma 67:257–264

    CAS  Google Scholar 

  • Sun P, Mao Y, Li G, Cao M, Kong F, Wang L, Bi G (2015) Comparative transcriptome profiling of Pyropia yezoensis (Ueda) MS Hwang & HG Choi in response to temperature stresses. BMC Genomics 16:463

    PubMed  PubMed Central  Google Scholar 

  • Sun LJ, Feng QM, Yan YF, Pan ZQ, Li XH, Song FM, Yang H, Xu JJ, Bao N, Gu HY (2014) Paper-based electroanalytical devices for in situ determination of salicylic acid in living tomato leaves. Biosens Bioelectron 60:154–160

    CAS  PubMed  Google Scholar 

  • Sun LJ, Xie Y, Yan YF, Yang H, Gu HY, Bao N (2017) Paper-based analytical devices for direct electrochemical detection of free IAA and SA in plant samples with the weight of several milligrams. Sensor Actuat B 247:336–342

    CAS  Google Scholar 

  • Tarakhovskaya ER, Maslov YI, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physl 54:163–170

    CAS  Google Scholar 

  • Tu S, Yang R, Xu X, Chen J, Luo Q, Zhu Z, Chen H, Yan X (2017) Flg22-triggered oxylipin production in Pyropia haitanensis. Phycol Res 65:86–93

    CAS  Google Scholar 

  • Uji T, Matsuda R, Takechi K, Takano H, Mizuta H, Takio S (2016) Ethylene regulation of sexual reproduction in the marine red alga Pyropia yezoensis (Rhodophyta). J Appl Phycol 28:3501–3509

    CAS  Google Scholar 

  • Uji T, Gondaira Y, Fukuda S, Mizuta H, Saga N (2019) Characterization and expression profiles of small heat shock proteins in the marine red alga Pyropia yezoensis. Cell Stress Chaperon 24:223–233

    CAS  Google Scholar 

  • Wang X, Chen H, Chen J, Luo Q, Xu J, Yan X (2013) Response of Pyropia haitanensis to agaro-oligosaccharides evidenced mainly by the activation of the eicosanoid pathway. J Appl Phycol 25:1895–1902

    CAS  Google Scholar 

  • Wang W, Teng F, Lin Y, Ji D, Xu Y, Chen C, Xie C (2018) Transcriptomic study to understand thermal adaptation in a high temperature-tolerant strain of Pyropia haitanensis. PLoS One 13:e0195842

    PubMed  PubMed Central  Google Scholar 

  • Yokoya NS, Ávila M, Piel MI, Villanueva F, Alcapan A (2014) Effects of plant growth regulators on growth and morphogenesis in tissue culture of Chondracanthus chamissoi (Gigartinales, Rhodophyta). J Appl Phycol 26:819–823

    CAS  Google Scholar 

  • Zhan Z, Wang W, Zhang G (2016) Risk analysis of aluminium contamination in kelp and laver. J Food Safety Quality 7:1330–1334

    Google Scholar 

  • Zhu ZB, Sun X, Xu NJ, Luo QJ (2012) Effects of salicylic acid on the resistance of Gracilaria/Gracilariopsis lemaneiformis to high temperature. J Fish China 8:021

    Google Scholar 

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Acknowledgments

We would like to thank LetPub (www.letpub.com) for providing linguistic assistance during the preparation of this manuscript.

Funding

This work was supported by Zhejiang Public welfare technology application research (analysis test) project (Grant No. 2017C37053), National Natural Science Foundation of China (Grant No. 31600986, 31770399, and 31400315), K.C. Wong Magna Fund in Ningbo University.

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Author notes

  1. Qiong Wang, Xiaohui Li and Lingjuan Tang contributed equally to this work.

Authors and Affiliations

  1. Marine Environmental Monitoring Center of Ningbo, State Oceanic Administration, Ningbo, 315012, Zhejiang, China

    Qiong Wang & Yuejun Fei

  2. College of Food and Pharmaceutical Sciences, Ningbo University, Ningbo, 315832, Zhejiang, China

    Xiaohui Li

  3. Analysis and Testing Center, Nantong University, Nantong, 226019, Jiangsu, China

    Lingjuan Tang & Yu Pan

  4. School of Life Sciences, Nantong University, Nantong, 226019, Jiangsu, China

    Lijun Sun

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  1. Qiong Wang
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Contributions

XL and QW designed the experiments. QW and LT performed the experiments. QW, YP, and YF analyzed the data. XL and LS drafted the initial manuscript. All the authors agreed on the contents of the paper. All the authors read and approved the final manuscript.

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Correspondence to Xiaohui Li or Lijun Sun.

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Supplementary Fig. 1

The variation of IAA and SA levels under control condition in P. haitanensis thallus. (A) in situ DPV detection of IAA and SA levels at different times under control condition in P. haitanensis thallus. (B) Histogram of IAA levels at different times under control condition. (C) Histogram of SA levels at different times under control condition. (D) (E) Expression levels of P. haitanensis PhNIT and PhCHS mRNA relative to Ph18S mRNA in P. haitanensis thallus. Means ± SEM are relative values obtained from three biological replicates; different letters represent significant differences (P < 0.05, Student’s t test). (PPTX 1599 kb)

Supplementary Fig. 2

Detection results of IAA and SA using HPLC-MS after high temperature exposure of P. haitanensis thallus. The thalli treated with high temperature for different times were extracted and analyzed by LC-MS. The quantity of IAA and SA were determined depending on standard curves. Means ± SEM are relative values obtained from three biological replicates; different letters represent significant differences (P < 0.05, Student’s t test). (PPTX 40 kb)

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Wang, Q., Li, X., Tang, L. et al. Paper-based electroanalytical devices for in situ determination of free 3-indoleacetic acid and salicylic acid in living Pyropia haitanensis thallus under various environmental stresses. J Appl Phycol 32, 485–497 (2020). https://doi.org/10.1007/s10811-019-01913-7

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