Rhizome trait scaling relationships are modulated by growth conditions and are linked to plant fitness
Language English Country Great Britain, England Media print
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
35180294
PubMed Central
PMC9007095
DOI
10.1093/aob/mcac023
PII: 6532026
Knihovny.cz E-resources
- Keywords
- Allometry, climate change, clonal grass, plasticity, resource allocation,
- MeSH
- Biomass MeSH
- Festuca * MeSH
- Poaceae MeSH
- Rhizome * MeSH
- Climate MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND AND AIMS: Rhizomes are important organs allowing many clonal plants to persist and reproduce under stressful climates with longer rhizomes, indicating enhanced ability of the plants to spread vegetatively. We do not, however, know either how rhizome construction costs change with increasing length or how they vary with environmental conditions. METHODS: We analysed the rhizome length vs. mass scaling relationship, the plasticity in the scaling relationships, their genetic basis and how scaling relationships are linked to plant fitness. We used data from 275 genotypes of a clonal grass Festuca rubra originating from 11 localities and cultivated under four contrasting climates. Data were analysed using standard major axis regression, mixed-effect regression models and a structural equation model. KEY RESULTS: Rhizome construction costs increased (i.e. lower specific rhizome length) with increasing length. The trait scaling relationships were modulated by cultivation climate, and its effects also interacted with the climate of origin of the experimental plants. With increasing length, increasing moisture led to a greater increase in rhizome construction costs. Plants with lower rhizome construction costs showed significantly higher fitness. CONCLUSIONS: This study suggests that rhizome scaling relationships are plastic, but also show genetic differentiation and are linked to plant fitness. Therefore, to persist under variable environments, modulation in scaling relationships could be an important plant strategy.
Department of Botany Faculty of Science Charles University Prague Czech Republic
Institute of Botany Czech Academy of Sciences Czech Republic
See more in PubMed
Anderson JT. 2016. Plant fitness in a rapidly changing world. New Phytologist 210: 81–87. PubMed
Atkin OK, Atkinson LJ, Fisher RA, et al. . 2008. Using temperature-dependent changes in leaf scaling relationships to quantitatively account for thermal acclimation of respiration in a coupled global climate–vegetation model. Global Change Biology 14: 2709–2726.
Balestri E, Lardicci C. 2014. Seagrass response to burial and breakage of expanding horizontal rhizomes: implications for clone spread. Marine Ecology Progress Series 504: 133–145.
Barrett P. 2007. Structural equation modelling: adjudging model fit. Personality and Individual Differences 42: 815–824.
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67.
Billings WD, Mooney HA. 1968. The ecology of arctic and alpine plants. Biological Reviews 43: 481–529.
Buermann W, Forkel M, O’Sullivan M, et al. . 2018. Widespread seasonal compensation effects of spring warming on northern plant productivity. Nature 562: 110–114. PubMed
Casasa S, Moczek AP. 2019. Evolution of, and via, developmental plasticity: insights through the study of scaling relationships. Integrative and Comparative Biology 59: 1346–1355. PubMed
Chen G, Hobbie SE, Reich PB, Yang Y, Robinson D. 2019. Allometry of fine roots in forest ecosystems. Ecology Letters 22: 322–331. PubMed
Coughlan J, Coughlan J, Mullen M. 2008. Structural equation modeling : guidelines for determining model fit. Electronic Journal of Business Research Methods 6: 53–60.
Datta A, Kühn I, Ahmad M, Michalski S, Auge H. 2017. Processes affecting altitudinal distribution of invasive Ageratina adenophora in western Himalaya: the role of local adaptation and the importance of different life-cycle stages. PLoS One 12: e0187708. PubMed PMC
De Deyn GB, Cornelissen JHC, Bardgett RD. 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters 11: 516–531. PubMed
Deng Q, Yuan Z, Shi X, Lock TR, Kallenbach RL. 2020. Testing allometric scaling relationships in plant roots. Forest Ecosystems 7: 1–11.
Díaz S, Kattge J, Cornelissen JHC, et al. . 2016. The global spectrum of plant form and function. Nature 529: 167–171. PubMed
Duchoslavová J, Jansa J. 2018. The direction of carbon and nitrogen fluxes between ramets in Agrostis stolonifera changes during ontogeny under simulated competition for light. Journal of Experimental Botany 69: 2149–2158. PubMed PMC
Enquist BJ, Norberg J, Bonser SP, et al. . 2015. Scaling from traits to ecosystems: developing a general trait driver theory via integrating trait-based and metabolic scaling theories. Advances in Ecological Research 52: 249–318.
Enquist BJ, Tiffney BH, Niklas KJ. 2007. Metabolic scaling and the evolutionary dynamics of plant size, form, and diversity: toward a synthesis of ecology, evolution, and paleontology. International Journal of Plant Sciences 168: 729–749.
Fajardo A. 2016. Are trait-scaling relationships invariant across contrasting elevations in the widely distributed treeline species Nothofagus pumilio? American Journal of Botany 103: 821–829. PubMed
Goldberg DE, Batzer E, Elgersma K, Martina J, Klimešová J. 2020. Allocation to clonal growth: critical questions and protocols to answer them. Perspectives in Plant Ecology, Evolution and Systematics 43: 125511.
Halbritter AH, Fior S, Keller I, et al. . 2018. Trait differentiation and adaptation of plants along elevation gradients. Journal of Evolutionary Biology 31: 784–800. PubMed
Hull JC. 2008. Plant ecology. In: Encyclopedia of ecology. Amsterdam: Elsevier, 2818–2824.
Hurlbert SH. 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54: 187–211.
Hurlbert SH. 2004. On misinterpretations of pseudoreplication and related matters: a reply to Oksanen. Oikos 104: 591–597.
Husáková I, Weiner J, Münzbergová Z. 2018. Species traits and shoot–root biomass allocation in 20 dry-grassland species. Journal of Plant Ecology 11: 273–285.
Jacobsen AL, Fickle JC, Castro V, Madsen A, Ennajeh M, Pratt RB. 2020. Node frequency alters stem biomechanics and hydraulics in four deciduous woody species. Journal of Wood Science 66: 26.
Johnson SN, Gherlenda AN, Frew A, Ryalls JMW. 2016. The importance of testing multiple environmental factors in legume–insect research: replication, reviewers, and rebuttal. Frontiers in Plant Science 7: 489. PubMed PMC
Kinmonth-Schultz H, Kim SH. 2011. Carbon gain, allocation and storage in rhizomes in response to elevated atmospheric carbon dioxide and nutrient supply in a perennial C 3 grass, Phalaris arundinacea. Functional Plant Biology 38: 797–807. PubMed
Klanderud K, Vandvik V, Goldberg D. 2015. The importance of biotic vs. abiotic drivers of local plant community composition along regional bioclimatic gradients. PLos One 10: e0130205. PubMed PMC
Klimeš L, Klimešová J, Čížková H. 1999. Carbohydrate storage in rhizomes of Phragmites australis: the effects of altitude and rhizome age. Aquatic Botany 64: 105–110.
Klimešová J, De Bello F. 2009. CLO‐PLA: the database of clonal and bud bank traits of Central European flora. Journal of Vegetation Science 20: 511–516.
Klimešová J, Janeček Š, Bartušková A, et al. . 2017. Is the scaling relationship between carbohydrate storage and leaf biomass in meadow plants affected by the disturbance regime? Annals of Botany 120: 979–985. PubMed PMC
Körner C. 2003. Alpine plant life: functional plant ecology of high mountain ecosystems. Berlin, Heidelberg: Springer Berlin Heidelberg.
Kosová V, Hájek T, Hadincová V, Munzbergová Z. 2022. The importance of ecophysiological traits in response of Festuca rubra to changing climate. Physiologia Plantarum 174. doi:10.1111/ppl.13608 PubMed DOI
Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC. 2016. Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. Journal of Ecology 104: 1299–1310.
Leishman MR, Haslehurst T, Ares A, Baruch Z. 2007. Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytologist 176: 635–643. PubMed
Liu Y, Dawson W, Prati D, Haeuser E, Feng Y, Van Kleunen M. 2016. Does greater specific leaf area plasticity help plants to maintain a high performance when shaded? Annals of Botany 118: 1329–1336. PubMed PMC
Lopez F, Acosta FJ, Serrano JM. 1994. Guerilla vs. phalanx strategies of resource capture: growth and structural plasticity in the trunk trail system of the harvester ant Messor barbarus. Journal of Animal Ecology 63: 127.
Manzanedo RD, Fischer M, María Navarro-Cerrillo R, Allan E. 2019. A new approach to study local adaptation in long‐lived woody species: virtual transplant experiments. Methods in Ecology and Evolution 10: 1761–1772.
Meyer AH, Schmid B. 1999. Experimental demography of rhizome populations of establishing clones of Solidago altissima. Journal of Ecology 87: 42–54.
Milla R, Reich PB. 2007. The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proceedings of the Royal Society B: Biological Sciences 274: 2109–2114. PubMed PMC
Mota CF, Engelen AH, Serrao EA, et al. . 2018. Differentiation in fitness-related traits in response to elevated temperatures between leading and trailing edge populations of marine macrophytes. PLoS One 13: e0203666. PubMed PMC
Münzbergová Z, Hadincová V, Skálová H, Vandvik V. 2017. Genetic differentiation and plasticity interact along temperature and precipitation gradients to determine plant performance under climate change. Journal of Ecology 105: 1358–1373.
Münzbergová Z, Latzel V, Šurinová M, Hadincová V. 2019. DNA methylation as a possible mechanism affecting ability of natural populations to adapt to changing climate. Oikos 128: 124–134.
Natali SM, Schuur EAG, Rubin RL. 2012. Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost. Journal of Ecology 100: 488–498.
Niklas KJ, Cobb ED, Niinemets Ü, et al. . 2007. ‘Diminishing returns’ in the scaling of functional leaf traits across and within species groups. Proceedings of the National Academy of Sciences, USA 104: 8891–8896. PubMed PMC
Niklas KJ, Enquist BJ. 2001. Invariant scaling relationships for interspecific plant biomass production rates and body size. Proceedings of the National Academy of Sciences, USA 98: 2922–2927. PubMed PMC
Oksanen L. 2001. Logic of experiments in ecology: is pseudoreplication a pseudoissue? Oikos 94: 27–38.
Ott JP, Klimešová J, Hartnett DC. 2019. The ecology and significance of below-ground bud banks in plants. Annals of Botany 123: 1099–1118. PubMed PMC
Pan JJ, Price JS. 2001. Fitness and evolution in clonal plants: the impact of clonal growth. Evolutionary Ecology 15: 583–600.
Pedersen O, Sauter M, Colmer TD, Nakazono M. 2021. Regulation of root adaptive anatomical and morphological traits during low soil oxygen. New Phytologist 229: 42–49. PubMed
Poorter H, Jagodzinski AM, Ruiz-Peinado R, et al. . 2015. How does biomass distribution change with size and differ among species? An analysis for 1200 plant species from five continents. New Phytologist 208: 736–749. PubMed PMC
Price CA, Enquist BJ. 2007. Scaling mass and morphology in leaves: an extension of the WBE model. Ecology 88: 1132–1141. PubMed
R Core Team. 2019. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Reich PB. 2014. The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102: 275–301.
Reich PB, Walters MB, Ellsworth DS. 1997. From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences, USA 94: 13730–13734. PubMed PMC
Rosseel Y. 2012. lavaan : an R package for structural equation modeling. Journal of Statistical Software 48: doi: 10.18637/jss.v048.i02 DOI
Säfken B, Rügamer D, Kneib T, Greven S. 2021. Conditional model selection in mixed-effects models with cAIC4. Journal of Statistical Software 99: 1–30. doi:10.18637/jss.v099.i08 DOI
Schermelleh-Engel K, Moosbrugger H, Müller H. 2003. Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. MPR-Online 8: 23–74.
Silver WL, Miya RK. 2001. Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129: 407–419. PubMed
Skálová H, Pecháčková S, Suzuki J, et al. . 1997. Within population genetic differentiation in traits affecting clonal growth: Festuca rubra in a mountain grassland. Journal of Evolutionary Biology 10: 383–406.
Speed JDM, Cooper EJ, Jónsdóttir IS, Van Der Wal R, Woodin SJ. 2010. Plant community properties predict vegetation resilience to herbivore disturbance in the Arctic. Journal of Ecology 98: 1002–1013.
Springate DA, Kover PX. 2014. Plant responses to elevated temperatures: a field study on phenological sensitivity and fitness responses to simulated climate warming. Global Change Biology 20: 456–465. PubMed PMC
Stojanova B, Šurinová M, Klápště J, Koláříková V, Hadincová V, Münzbergová Z. 2018. Adaptive differentiation of Festuca rubra along a climate gradient revealed by molecular markers and quantitative traits. PLoS One 13: 1–20. PubMed PMC
Striker GG, Insausti P, Grimoldi AA, Leon RJC. 2006. Root strength and trampling tolerance in the grass Paspalum dilatatum and the dicot Lotus glaber in flooded soil. Functional Ecology 20: 4–10.
Šurinová M, Hadincová V, Vandvik V, Münzbergová Z. 2019. Temperature and precipitation, but not geographic distance, explain genetic relatedness among populations in the perennial grass Festuca rubra. Journal of Plant Ecology 12: 730–741.
Thakur D, Rathore N, Chawla A. 2019. Increase in light interception cost and metabolic mass component of leaves are coupled for efficient resource use in the high altitude vegetation. Oikos 128: 254–263.
Vasseur F, Exposito-Alonso M, Ayala-Garay OJ, et al. . 2018. Adaptive diversification of growth allometry in the plant Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 115: 3416–3421. PubMed PMC
Velásquez AC, Castroverde CDM, He SY. 2018. Plant–pathogen warfare under changing climate conditions. Current Biology 28: R619–R634. PubMed PMC
Warton DI, Duursma RA, Falster DS, Taskinen S. 2012. smatr 3 – an R package for estimation and inference about allometric lines. Available at: https://besjournals.onlinelibrary.wiley.com/doi/epdf/10.1111/j.2041-210X.2011.00153.x. Accessed 25 January 2021. DOI
Weiher E, Clarke GDP, Keddy PA. 1998. Community assembly rules, morphological dispersion, and the coexistence of plant species. Oikos 81: 309–322.
Wild J, Kopecký M, Macek M, Šanda M, Jankovec J, Haase T. 2019. Climate at ecologically relevant scales: a new temperature and soil moisture logger for long-term microclimate measurement. Agricultural and Forest Meteorology 268: 40–47.
Wright IJ, Reich PB, Cornelissen JHC, et al. . 2005. Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography 14: 411–421.
Wright IJ, Reich PB, Westoby M, et al. . 2004. The worldwide leaf economics spectrum. Nature 428: 821–827. PubMed
Xiang S, Reich PB, Sun S, Atkin OK. 2013. Contrasting leaf trait scaling relationships in tropical and temperate wet forest species. Functional Ecology 27: 522–534.
Yan ER, Wang XH, Chang SX, He F. 2013. Scaling relationships among twig size, leaf size and leafing intensity in a successional series of subtropical forests. Tree Physiology 33: 609–617. PubMed
Ye XH, Yu FH, Dong M. 2006. A trade-off between guerrilla and phalanx growth forms in Leymus secalinus under different nutrient supplies. Annals of Botany 98: 187–191. PubMed PMC
Younginger BS, Sirová D, Cruzan MB, Ballhorn DJ. 2017. Is biomass a reliable estimate of plant fitness? Applications in Plant Sciences 5: 1600094. PubMed PMC