Abstract
Key message
This article describes the root exudation of proline and phytohormones in citrus and their involvement in salt- and heat-stress responses.
Abstract
Plants are constantly releasing several compounds to the rhizosphere through their roots, including primary and secondary metabolites. Root exudation can be affected by growth conditions, including pH, nutrient availability, soil salinity, or temperature. In vitro-cultured plants of two citrus genotypes with contrasting tolerance to salt- and heat-stress conditions were used as plant material. Proline and phytohormone contents in root exudates from plants subjected to salt or high-temperature conditions were evaluated. In addition, tissue damage and lipid peroxidation together with endogenous levels of chloride, proline, and phytohormones were determined in roots and shoots. Proline was released in larger quantities to the rhizosphere when plants were subjected to salt or heat stress. In each stress condition, the concentration of this amino acid was higher in the exudates obtained from plants tolerant to this particular stress condition. On the other hand, root exudation of phytohormones salicylic acid, indole acetic acid, abscisic acid, and jasmonic acid generally increased under both adverse conditions. Results confirm a phytohormone exudation in citrus plants, which had not been described previously and can have an important role in the rhizosphere communication. Moreover, stress conditions and the different tolerance of each genotype to the particular stress significantly modify the exudation pattern both quantitatively and qualitatively.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- AMF:
-
Arbuscular mycorrhizal fungi
- CC:
-
Citrange carrizo
- CIN:
-
t-Cinnamic acid
- CM:
-
Citrus macrophylla
- IAA:
-
3-Indole acetic acid
- JA:
-
Jasmonic acid
- MDA:
-
Malondialdehyde
- RWC:
-
Relative water content
- SA:
-
Salicylic acid
References
Arbona V, Hossain Z, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466
Arbona V, Manzi M, de Ollas C, Gómez-Cadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14:4885–4911
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681
Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
Carvalhais LC, Dennis PG, Schenk PM (2014) Plant defence inducers rapidly influence the diversity of bacterial communities in a potting mix. Appl Soil Ecol 84:1–5
Dardanelli MS, Manyani H, González-Barroso S, Rodríguez-Carvajal MA, Gil-Serrano AM, Espuny MR, López-Baena FJ, Bellogín RA, Megías M, Ollero FJ (2010) Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328:483–493
Dardanelli MS, Fernández de Córdoba FJ, Estévez J, Contreras R, Cubo MT, Rodríguez-Carvajal MA, Gil-Serrano AM, López-Baena FJ, Bellogín RA, Manyani H, Ollero FJ, Megías M (2012) Changes in flavonoids secreted by Phaseolus vulgaris roots in the presence of salt and the plant growth-promoting rhizobacterium Chryseobacterium balustinum. Appl Soil Ecol 57:31–38
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 Plant 147:296–306
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
Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography–electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442
Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743
García-Legaz MF, Ortiz JM, García-Lidón A, Cerdá A (1993) Effect of salinity on growth, ion content and CO2 assimilation rate in lemon varieties on different rootstocks. Physiol Plant 89:427–432
Gómez-cadenas A, Vives V, Zandalinas SI, Manzi M, Sánchez-Pérez AM, Pérez-Clemente RM, Arbona V (2015) Abscisic acid: a versatile phytohormone in plant signaling and beyond. Curr Protein Pept Sci 16:413–434
Henry A, Doucette W, Norton J, Bugbee B (2007) Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress. J Environ Qual 36:904–912
Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Hussain S, Luro F, Costantino G, Ollitrault P, Morillon R (2012) Physiological analysis of salt stress behaviour of citrus species and genera: low chloride accumulation as an indicator of salt tolerance. South Afr J Bot 81:103–112
Iglesias DJ, Levy Y, Gómez-Cadenas A, Tadeo FR, Primo-Millo E, Talon M (2004) Nitrate improves growth in salt-stressed citrus seedlings through effects on photosynthetic activity and chloride accumulation. Tree Physiol 24:1027–1034
Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. Arab B e0153
Khorassani R, Hettwer U, Ratzinger A, Steingrobe B, Karlovsky P, Claassen N (2011) Citramalic acid and salicylic acid in sugar beet root exudates solubilize soil phosphorus. BMC Plant Biol 11:121
Kumar RR, Goswani S, Sharma SK, Singh K, Gadpayle KA, Kumar N, Rai GK, Singh M, Rai RD (2012) Protection against heat stress in wheat involves change in cell membrane stability, antioxidant enzymes, osmolyte, H2O2 and transcript of heat shock protein. Int J Plant Physiol Biochem 4:83–91
Leveau JHJ, Lindow SE (2005) Utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida Strain 1290. Appl Environ Microbiol 71:2365–2371
López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 62:176–184
Marin JA, Andreu P, Carrasco A, Arbeloa A (2010) Determination of proline concentration, an abiotic stress marker, in root exudates of excised root cultures of fruit tree rootstocks under salt stress. Rev Des Régions Arid 24:722–727
Montoliu A, López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2009) A novel in vitro tissue culture approach to study salt stress responses in citrus. Plant Growth Regul 59:179–187
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Otero A, Goñi C, Syverstsen JP (2015) Flooding and soil temperature affect water relations and photosynthesis of citrus rootstock leaves. Acta Hortic 1065:1399–1406
Pérez-Clemente RM, Montoliu A, Zandalinas SI, De Ollas C, Gómez-Cadenas A (2012) Carrizo citrange plants do not require the presence of roots to modulate the response to osmotic stress. Sci World J 2012:1–13
Regvar M, Gogala N, Zalar P (1996) Effect of jasmonic acid on mycorrhizal Allium sativum. New Phytol 134:703–707
Saadia M, Jamil A, Akram NA, Ashraf M (2012) A study of proline metabolism in canola (Brassica napus L.) seedlings under salt stress. Molecules 17:5803–5815
Segura A, Hernández-Sánchez V, Marqués S, Molina L (2017) Insights in the regulation of the degradation of PAHs in Novosphingobium sp. HR1a and utilization of this regulatory system as a tool for the detection of PAHs. Sci Total Environ 590–591:381–393
Tawaraya K, Horie R, Akiko S, Shinano T, Wagatsuma T, Saito K, Oikawa A (2013) Metabolite profiling of shoot extracts, root extracts, and root exudates of rice plant under phosphorus deficiency. J Plant Nutr 36:1138–1159
Tawaraya K, Horie R, Shinano T, Wagatsuma T, Saito K, Oikawa A (2014) Metabolite profiling of soybean root exudates under phosphorus deficiency. Soil Sci Plant Nutr 60:679–694
Trivedi P, Spann T, Wang N (2011) Isolation and characterization of beneficial bacteria associated with citrus roots in Florida. Microb Ecol 62:324–336
Valentinuzzi F, Pii Y, Vigani G, Lehmann M, Cesco S, Mimmo T (2015) Phosphorus and iron defciencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria x ananassa. J Exp Bot 66:6483–6495
Valenzuela CE, Acevedo-Acevedo O, Miranda GS et al (2016) Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root. J Exp Bot 67:4209–4220
Vílchez S, Molina L, Ramos C, Ramos JL (2000) Proline catabolism by Pseudomonas putida: cloning, characterization, and expression of the put genes in the presence of root exudates. J Bacteriol 182:91–99
Vranova V, Rejsek K, Skene KR, Janous D, Formanek P (2013) Methods of collection of plant root exudates in relation to plant metabolism and purpose: a review. J Plant Nutr Soil Sci 176:175–199
Yao L, Wu Z, Zheng Y, Kallem I, Li C (2010) Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur J Soil Biol 46:49–54
Yazaki K, Sugiyama A, Morita M, Shitan N (2008) Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochem Rev 7:513–524
Zandalinas SI, Rivero RM, Martínez V, Gómez-Cadenas A, Arbona V (2016) Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biol 16:105
Zandalinas SI, Sales C, Beltrán J, Gómez-Cadenas A, Arbona V (2017) Activation of secondary metabolism in citrus plants is associated to sensitivity to combined drought and high temperatures. Front Plant Sci 7:Art. 1954
Acknowledgements
This work was supported by the Spanish Ministerio de Economia y Competitividad (MINECO) and Universitat Jaume I through Grant Nos. AGL2016-76574-R and UJI-B2016-23, respectively. V.V.-P. was recipient of a predoctoral contract from the Universitat Jaume I (PREDOC/2013/31).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Prakash P. Kumar.
Rights and permissions
About this article
Cite this article
Vives-Peris, V., Gómez-Cadenas, A. & Pérez-Clemente, R.M. Citrus plants exude proline and phytohormones under abiotic stress conditions. Plant Cell Rep 36, 1971–1984 (2017). https://doi.org/10.1007/s00299-017-2214-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-017-2214-0