Transportation or sharing of stress signals among interconnected ramets improves systemic resistance of clonal networks to water stress
Qing Wei
A , Qian Li A , Yu Jin A , Shulan Wu A , Lihua Fan A , Ningfei Lei B C and Jinsong Chen A C
+ Author Affiliations
- Author Affiliations
A College of Life Science, Sichuan Normal University, Chengdu 610 000, China.
B College of Environment, Chengdu University of Technology, Chengdu 610 000, China.
C Corresponding authors. Emails: 470226504@qq.com; cjs74@163.com
Functional Plant Biology 46(7) 613-623 https://doi.org/10.1071/FP18232
Submitted: 28 August 2018 Accepted: 21 February 2019 Published: 23 April 2019
Abstract
Previous studies have elucidated the mechanisms, ecological implications and constraints on transportation or sharing of defence signals among interconnected ramets of clonal plants suffering from localised herbivore damage. To our knowledge, few studies have been conducted to provide insights into the ecological implications on transportation or sharing of stress signals for clonal plants subjected to water stress. As a chemical elicitor, ABA can induce resistance response in plants suffering from water stress. A pot experiment was conducted to explore transportation or sharing of stress signals among interconnected ramets by using clonal fragments of Centella asiaticas (L.) Urban with four successive ramets (oldest, old, mature and young) subjected to low water availability (20% soil moisture contents). Compared with control, foliar oxidative stress of the old, mature and young ramets significantly decreased, and antioxidant capacity was increased when exogenous ABA was applied to the oldest ramets. Meanwhile, foliar PSII activity and chlorophyll content of the old, mature and young ramets significantly increased. Compared with control, biomass accumulation and ratio of below-ground/aboveground biomass of whole clonal fragments were significantly increased by ABA application to the oldest ramets. However, similar patterns were not observed when exogenous ABA was applied to the young ramets. Our results show that transportation or sharing of stress signals among interconnected ramets improves systemic resistance of clonal networks to water stress, which is dependent on directionality of vascular flows. Compared with the old or mature ramets, the young ramets displayed stronger resistance response (such as higher antioxidant enzymes activities and proline content, lower O2•− production rate and malondialdehyde content) to water stress as well as higher PSII activity and chlorophyll content when exogenous ABA was applied to the oldest ramets. Thus, transportation or sharing of stress signals may favour young ramets that are most valuable for growth and fitness of clonal plant subjected to environmental stress. It is suggested that transportation or sharing of stress signals among interconnected ramets may confer clonal plants with considerable benefits in adapting to spatio-temporal heterogeneous habitats.
Additional keywords: Centella asiaticas, clonal integration, exogenous ABA.
References
Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.| Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |
Ali HM, Siddiqui MH, Al-Whaibi MH, Basalah MO, Sakran AM, El-Zaidy M (2013) Effect of proline and abscisic acid on the growth and physiological performance of Faba bean under water stress. Pakistan Journal of Botany 45, 933–940.
Alpert P, Holzapfel C, Benson JM (2002) Hormonal modification of resource sharing in the clonal plant Fragaria chiloensis. Functional Ecology 16, 191–197.
| Hormonal modification of resource sharing in the clonal plant Fragaria chiloensis.Crossref | GoogleScholarGoogle Scholar |
Athar HR, Zafar ZU, Ashraf M (2015) Glycinebetaine improved photosynthesis in canola under salt stress: evaluation of chlorophyll fluorescence parameters as potential indicators. Journal Agronomy & Crop Science 201, 428–442.
| Glycinebetaine improved photosynthesis in canola under salt stress: evaluation of chlorophyll fluorescence parameters as potential indicators.Crossref | GoogleScholarGoogle Scholar |
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
| Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Bråthen KA, Agrell J, Berteaux D, Jónsdóttir IS (2004) Intraclonal variation in defence substances and palatability: a study on Carex and lemmings. Oikos 105, 461–470.
| Intraclonal variation in defence substances and palatability: a study on Carex and lemmings.Crossref | GoogleScholarGoogle Scholar |
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiology 98, 1222–1227.
| Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves.Crossref | GoogleScholarGoogle Scholar | 16668779PubMed |
Chen JS, Lei NF, Dong M (2010) Clonal integration improves the tolerance of Carex praeclara to sand burial by compensatory response. Acta Oecologica 36, 23–28.
| Clonal integration improves the tolerance of Carex praeclara to sand burial by compensatory response.Crossref | GoogleScholarGoogle Scholar |
Chen JS, Lei NF, Liu Q (2011) Defense signaling among interconnected ramets of a rhizomatous clonal plant, induced by jasmonic-acid application. Acta Oecologica 37, 355–360.
| Defense signaling among interconnected ramets of a rhizomatous clonal plant, induced by jasmonic-acid application.Crossref | GoogleScholarGoogle Scholar |
Chen JS, Li J, Zhang Y, Zong H, Lei NF (2015) Clonal integration ameliorates the carbon accumulation capacity of a stoloniferous herb, Glechoma longituba, growing in heterogenous light conditions by facilitating nitrogen assimilation in the rhizosphere. Annals of Botany 115, 127–136.
| Clonal integration ameliorates the carbon accumulation capacity of a stoloniferous herb, Glechoma longituba, growing in heterogenous light conditions by facilitating nitrogen assimilation in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 25429006PubMed |
Chinese Academy of Sciences (2004) jing
Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signaling & Behavior 8, e23681
| Reactive oxygen species signaling in plants under abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. The Plant Journal 90, 856–867.
| Reactive oxygen species, abiotic stress and stress combination.Crossref | GoogleScholarGoogle Scholar | 27801967PubMed |
Dias MC, Correia C, Moutinho-Pereira J, Oliveira H, Santos C (2014) Study of the effects of foliar application of ABA during acclimatization. Plant Cell, Tissue and Organ Culture 117, 213–224.
| Study of the effects of foliar application of ABA during acclimatization.Crossref | GoogleScholarGoogle Scholar |
Dong BC, Alpert P, Zhang Q, Yu FH (2015) Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides. Oecologia 179, 393–403.
| Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides.Crossref | GoogleScholarGoogle Scholar | 26009243PubMed |
Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, de Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytologist 180, 722–734.
| Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate.Crossref | GoogleScholarGoogle Scholar | 18721163PubMed |
Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) Invitro reconstitution of an ABA signaling pathway. Nature 462, 660–664.
| Invitro reconstitution of an ABA signaling pathway.Crossref | GoogleScholarGoogle Scholar | 19924127PubMed |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314.
| Superoxide dismutases: I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 16659839PubMed |
Gómez S, Stuefer JF (2006) Members only: induced systemic resistance to herbivory in a clonal plant network. Oecologia 147, 461–468.
| Members only: induced systemic resistance to herbivory in a clonal plant network.Crossref | GoogleScholarGoogle Scholar | 16333642PubMed |
Gómez S, Latzel V, Verhulst YM, Stuefer JF (2007) Costs and benefits of induced resistance in a clonal plant network. Oecologia 153, 921–930.
| Costs and benefits of induced resistance in a clonal plant network.Crossref | GoogleScholarGoogle Scholar | 17609982PubMed |
Gómez S, Onoda Y, Ossipov V, Stuefer JF (2008) Systemic induced resistance: a risk‐spreading strategy in clonal plant networks? New Phytologist 179, 1142–1153.
| Systemic induced resistance: a risk‐spreading strategy in clonal plant networks?Crossref | GoogleScholarGoogle Scholar | 18627496PubMed |
Gómez S, Van Dijk W, Stuefer JF (2010) Timing of induced resistance in a clonal plant network. Plant Biology 12, 512–517.
| Timing of induced resistance in a clonal plant network.Crossref | GoogleScholarGoogle Scholar | 20522188PubMed |
Guo DL, Liang JH, Li L (2009) Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L. Plant Growth Regulation 58, 173–179.
| Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L.Crossref | GoogleScholarGoogle Scholar |
Hazrati S, Tahmasebi-Sarvestani Z, Modarres-Sanavy SA, Mokhtassi-Bidgoli A, Nicola S (2016) Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L. Plant Physiology and Biochemistry 106, 141–148.
| Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L.Crossref | GoogleScholarGoogle Scholar | 27161580PubMed |
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
| Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |
Hussain S, Saleem MF, Iqbal J, Ibrahim M, Atta S, Ahmed T, Rehmani MIA (2014) Exogenous application of abscisic acid may improve the growth and yield of sunflower hybrids under drought. Pakistan Journal of Agricultural Sciences 51, 49–58.
Jelínková H, Tremblay F, Desrochers A (2012) Herbivore-simulated induction of defenses in clonal networks of trembling aspen (Populus tremuloides). Tree Physiology 32, 1348–1356.
| Herbivore-simulated induction of defenses in clonal networks of trembling aspen (Populus tremuloides).Crossref | GoogleScholarGoogle Scholar | 23065192PubMed |
Koubek T, Herben T (2008) Effect of systemic diseases on clonal integration: modelling approach. Evolutionary Ecology 22, 449–460.
| Effect of systemic diseases on clonal integration: modelling approach.Crossref | GoogleScholarGoogle Scholar |
Latif HH (2014) Physiological responses of Pisum sativum plant to exogenous ABA application under drought conditions. Pakistan Journal of Botany 46, 973–982.
Li CN, Yang LT, Srivastava MK, Li YR (2014) Foliar application of abscisic acid improves drought tolerance of sugarcane plant under severe water stress. International Journal of Agriculture Innovation and Research 3, 101–107.
Liu C, Wang Y, Pan K, Li W, Zhang L, Shen X, Liu L, Deng M (2014) Responses of the antioxidant defense system to drought stress in the leaves of Fargesia denudata seedlings, the staple food of the giant panda. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 61, 374–383.
| Responses of the antioxidant defense system to drought stress in the leaves of Fargesia denudata seedlings, the staple food of the giant panda.Crossref | GoogleScholarGoogle Scholar |
Ma XW, Ma FW, Mi YF, Ma YH, Shu HR (2008) Morphological and physiological responses of two contrasting malus species to exogenous abscisic acid application. Plant Growth Regulation 56, 77–87.
| Morphological and physiological responses of two contrasting malus species to exogenous abscisic acid application.Crossref | GoogleScholarGoogle Scholar |
McAdam SA, Brodribb TJ, Ross JJ (2016) Shoot derived abscisic acid promotes root growth. Plant, Cell & Environment 39, 652–659.
| Shoot derived abscisic acid promotes root growth.Crossref | GoogleScholarGoogle Scholar |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 12234732PubMed |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.
Peuke AD (2016) ABA flow modelling in Ricinus communis exposed to salt stress and variable nutrition. Journal of Experimental Botany 67, 5301–5311.
| ABA flow modelling in Ricinus communis exposed to salt stress and variable nutrition.Crossref | GoogleScholarGoogle Scholar | 27440939PubMed |
Ploenlap P, Pattanagul W (2015) Effects of exogenous abscisic acid on foliar anthocyanin accumulation and drought tolerance in purple rice. Biologia 70, 915–921.
| Effects of exogenous abscisic acid on foliar anthocyanin accumulation and drought tolerance in purple rice.Crossref | GoogleScholarGoogle Scholar |
Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends in Plant Science 15, 395–401.
| ABA perception and signalling.Crossref | GoogleScholarGoogle Scholar | 20493758PubMed |
Roiloa SR, Hutchings MJ (2012) The effects of rooting frequency and position of rooted ramets on plasticity and yield in a clonal species: an experimental study with Glechoma hederacea. Ecological Research 27, 145–152.
| The effects of rooting frequency and position of rooted ramets on plasticity and yield in a clonal species: an experimental study with Glechoma hederacea.Crossref | GoogleScholarGoogle Scholar |
Roiloa SR, Antelo B, Retuerto R (2014) Physiological integration modifies δ15N in the clonal plant Fragaria vesca, suggesting preferential transport of nitrogen to water-stressed offspring. Annals of Botany 114, 399–411.
| Physiological integration modifies δ15N in the clonal plant Fragaria vesca, suggesting preferential transport of nitrogen to water-stressed offspring.Crossref | GoogleScholarGoogle Scholar | 24769538PubMed |
Saitoh T, Seiwa K, Nishiwaki A (2006) Effects of resource heterogeneity on nitrogen translocation within clonal fragments of Sasa palmata: an isotopic (15N) assessment. Annals of Botany 98, 657–663.
| Effects of resource heterogeneity on nitrogen translocation within clonal fragments of Sasa palmata: an isotopic (15N) assessment.Crossref | GoogleScholarGoogle Scholar | 16845138PubMed |
Secchi F, Perrone I, Chitarra W, Zwieniecka AK, Lovisolo C, Zwieniecki MA (2013) The dynamics of embolism refilling in abscisic acid (ABA)-deficient tomato plants. International Journal of Molecular Sciences 14, 359–377.
| The dynamics of embolism refilling in abscisic acid (ABA)-deficient tomato plants.Crossref | GoogleScholarGoogle Scholar |
Song W, Ma X, Tan H, Zhou J (2011) Abscisic acid enhances resistance to Alternaria solani in tomato seedlings. Plant Physiology and Biochemistry 49, 693–700.
| Abscisic acid enhances resistance to Alternaria solani in tomato seedlings.Crossref | GoogleScholarGoogle Scholar | 21530290PubMed |
Stuefer JF, Gómez S, van Mölken T (2004) Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks. Evolutionary Ecology 18, 647–667.
| Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks.Crossref | GoogleScholarGoogle Scholar |
Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K (2018) A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556, 235–238.
| A small peptide modulates stomatal control via abscisic acid in long-distance signalling.Crossref | GoogleScholarGoogle Scholar | 29618812PubMed |
Teng K, Li J, Lei L, Han Y, Du Y, Jing Z, Sun H, Zhao Q (2014) Exogenous ABA induces drought tolerance in upland rice: the role of chloroplast and ABA biosynthesis-related gene expression on photosystem II during PEG stress. Acta Physiologiae Plantarum 36, 2219–2227.
| Exogenous ABA induces drought tolerance in upland rice: the role of chloroplast and ABA biosynthesis-related gene expression on photosystem II during PEG stress.Crossref | GoogleScholarGoogle Scholar |
Touchette BW, Moody JWG, Byrne CM, Marcus SE (2013) Water integration in the clonal emergent hydrophyte, Justicia americana: benefits of acropetal water transfer from mother to daughter ramets. Hydrobiologia 702, 83–94.
| Water integration in the clonal emergent hydrophyte, Justicia americana: benefits of acropetal water transfer from mother to daughter ramets.Crossref | GoogleScholarGoogle Scholar |
Tworkoski T, Wisniewski M, Artlip T (2011) Application of BABA and s-ABA for drought resistance in apple. Journal of Applied Horticulture 13, 85–90.
Wang SH, Sui XL, Hu LP, Sun JL, Wei YX, Zhang ZX (2010) Effects of exogenous abscisic acid pre-treatment of cucumber (Cucumis sativus) seeds on seedling growth and water-stress tolerance. New Zealand Journal of Crop and Horticultural Science 38, 7–18.
| Effects of exogenous abscisic acid pre-treatment of cucumber (Cucumis sativus) seeds on seedling growth and water-stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Xu L, Wu X, Zhou ZF (2016) Effects of physiological integration and fertilization on heavy metal remediation in soil by a clonal grass. Polish Journal of Environmental Studies 25, 395–404.
| Effects of physiological integration and fertilization on heavy metal remediation in soil by a clonal grass.Crossref | GoogleScholarGoogle Scholar |
Zhang LL, He WM (2009) Consequences of ramets helping ramets: no damage and increased nutrient use efficiency in nurse ramets of Glechoma longituba. Flora 204, 182–188.
| Consequences of ramets helping ramets: no damage and increased nutrient use efficiency in nurse ramets of Glechoma longituba.Crossref | GoogleScholarGoogle Scholar |
Zhang X, Wang T, Li C (2005) Different responses of two contrasting wheat genotypes to abscisic acid application. Biologia Plantarum 49, 613–616.
| Different responses of two contrasting wheat genotypes to abscisic acid application.Crossref | GoogleScholarGoogle Scholar |
Zhang YC, Zhang QY, Sammul M (2012) Physiological integration ameliorates negative effects of drought stress in the clonal herb Fragaria orientalis. PLoS One 7, e44221
| Physiological integration ameliorates negative effects of drought stress in the clonal herb Fragaria orientalis.Crossref | GoogleScholarGoogle Scholar |
Zhang FP, Sussmilch F, Nichols DS, Cardoso AA, Brodribb TJ, Sam MA (2018) Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms. Journal of Experimental Botany 69, 1261–1267.
| Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms.Crossref | GoogleScholarGoogle Scholar | 29340606PubMed |
