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RESEARCH ARTICLE
Contents Vol 52(6)

Multivariate analysis reveals physiological trade-offs and synergies under light and nutrient gradients in the herbaceous species Agastache rugosa

Khairul Azree Rosli https://orcid.org/0009-0002-9150-3684 A * , Azizah Misran A , Latifah Saiful Yazan B and Puteri Edaroyati Megat Wahab A
+ Author Affiliations
- Author Affiliations

A Department of Crop Science, Faculty of Agriculture, Universiti Putra Malaysia, UPM Serdang 43400, Selangor, Malaysia.

B Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, UPM Serdang 43400, Selangor, Malaysia.

* Correspondence to: khairulazreerosli@gmail.com

Handling Editor: Ravinder Kumar

Functional Plant Biology 52, FP24323 https://doi.org/10.1071/FP24323
Submitted: 8 December 2024  Accepted: 20 May 2025  Published: 6 June 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Agastache rugosa is an herbaceous species that shows a high degree of phenotypic plasticity in response to light and nutrient gradients, but the coordination among its leaf structural, photosynthetic, and resource use traits remains unexplored in tropical environments. We investigated the functional traits and resource use efficiencies of A. rugosa under four nutrient levels nested within two light levels. Photosynthetic rates increased under high-light, while leaf temperatures remained stable (34–37°C) across treatments, suggesting effective thermoregulation. Unexpectedly, Rubisco content was 22.4% higher under low-light, intermediate nutrient levels, indicating a compensatory mechanism. Water use efficiency increased under high-light, whereas photosynthetic phosphorus and potassium use efficiencies were higher under low-light levels. Principal component analysis showed that light and nutrients explained 71.6% of trait variation, with distinctive clustering of resource use efficiencies. Hierarchical clustering identified three functional trait groups at 90% similarity levels, comprising photosynthetic, nutrient use, and water conservation mechanisms. The species showed tight coordination between CO2 supply and demand, with strong correlations between photosynthetic traits and resource use efficiencies. Our findings demonstrate that A. rugosa employs a suite of adaptive mechanisms to optimise resource acquisition and utilisation across heterogeneous environments, advancing our understanding of plant responses to multiple resource gradients.

Keywords: Agastache rugosa, gas exchange, light and nutrient gradients, photosynthetic traits, physiological plasticity, resource use efficiency, Rubisco abundance, thermoregulation.

References

Adet L, Rozendaal DMA, Tapi A, Zuidema PA, Vaast P, Anten NPR (2024) Genotypic differences in water deficit effects on leaf and crown traits in mature field-grown cocoa. Scientia Horticulturae 325, 112658.
| Crossref | Google Scholar |

Aerts R, Chapin III FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1-67.
| Crossref | Google Scholar |

Ali HE, Bucher SF (2022) Effect of drought and nutrient availability on invaded plant communities in a semi-arid ecosystem. Ecology and Evolution 12(9), e9296.
| Crossref | Google Scholar | PubMed |

An JH, Yuk HJ, Kim D-Y, Nho CW, Lee D, Ryu HW, Oh S-R (2018) Evaluation of phytochemicals in Agastache rugosa (Fisch. & C.A.Mey.) Kuntze at different growth stages by UPLC-QTof-MS. Industrial Crops and Products 112, 608-616.
| Crossref | Google Scholar |

Anand S, Pang E, Livanos G, Mantri N (2018) Characterization of physico-chemical properties and antioxidant capacities of bioactive honey produced from Australian grown Agastache rugosa and its correlation with colour and poly-phenol content. Molecules 23(1), 108.
| Crossref | Google Scholar | PubMed |

Bonjoch NP, Tamayo PR (2001) Protein content quantification by Bradford method. In ‘Handbook of plant ecophysiology techniques’. (Ed. MJ Reigosa Roger) pp. 283–295. (Springer: Netherlands)

Bouain N, Krouk G, Lacombe B, Rouached H (2019) Getting to the root of plant mineral nutrition: combinatorial nutrient stresses reveal emergent properties. Trends in Plant Science 24(6), 542-552.
| Crossref | Google Scholar | PubMed |

Bowley S (1999) ‘A hitchhiker’s guide to statistics in plant biology.’ (Any Old Subject Books: Guelph (ON))

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(1–2), 248-254.
| Crossref | Google Scholar | PubMed |

Cagnola JI, Ploschuk E, Benech-Arnold T, Finlayson SA, Casal JJ (2012) Stem transcriptome reveals mechanisms to reduce the energetic cost of shade-avoidance responses in tomato. Plant Physiology 160(2), 1110-1119.
| Crossref | Google Scholar | PubMed |

Carmo-Silva E, Scales JC, Madgwick PJ, Parry MAJ (2015) Optimizing rubisco and its regulation for greater resource use efficiency. Plant, Cell & Environment 38(9), 1817-1832.
| Crossref | Google Scholar | PubMed |

Chaves MM, Costa JM, Zarrouk O, Pinheiro C, Lopes CM, Pereira JS (2016) Controlling stomatal aperture in semi-arid regions—the dilemma of saving water or being cool? Plant Science 251, 54-64.
| Crossref | Google Scholar | PubMed |

Chitwood DH, Kumar R, Ranjan A, Pelletier JM, Townsley B, Ichihashi Y, Martinez CC, Zumstein K, Harada JJ, Maloof JN, Sinha N (2015) Light-induced indeterminacy alters shade-avoiding tomato leaf morphology. Plant Physiology 169(3), 2030-2047.
| Crossref | Google Scholar |

Coble AP, Cavaleri MA (2014) Light drives vertical gradients of leaf morphology in a sugar maple (Acer saccharum) forest. Tree Physiology 34(2), 146-158.
| Crossref | Google Scholar | PubMed |

Courbier S, Pierik R (2019) Canopy light quality modulates stress responses in plants. iScience 22, 441-452.
| Crossref | Google Scholar | PubMed |

Damián X, Ochoa-López S, Gaxiola A, Fornoni J, Domínguez CA, Boege K (2020) Natural selection acting on integrated phenotypes: covariance among functional leaf traits increases plant fitness. New Phytologist 225(1), 546-557.
| Crossref | Google Scholar | PubMed |

Flexas J, Díaz-Espejo A, Conesa MA, Coopman RE, Douthe C, Gago J, Gallé A, Galmés J, Medrano H, Ribas-Carbo M, Tomàs M, Niinemets Ü (2016) Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. Plant, Cell & Environment 39(5), 965-982.
| Crossref | Google Scholar | PubMed |

Freschet GT, Violle C, Bourget MY, Scherer-Lorenzen M, Fort F (2018) Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress. New Phytologist 219(4), 1338-1352.
| Crossref | Google Scholar | PubMed |

Grabsztunowicz M, Górski Z, Luciński R, Jackowski G (2015) A reversible decrease in ribulose 1,5-bisphosphate carboxylase/oxygenase carboxylation activity caused by the aggregation of the enzyme’s large subunit is triggered in response to the exposure of moderate irradiance-grown plants to low irradiance. Physiologia Plantarum 154(4), 591-608.
| Crossref | Google Scholar | PubMed |

Grime JP, Pierce S (2012) ‘The evolutionary strategies that shape ecosystems.’ (John Wiley & Sons)

Guo J, Li X, Wang Y, Hu W, Zhang L, Luo Z, Xu H, Chen L-S (2024) Magnesium deficiency induced leaf chlorosis affects plant growth, mineral concentration and fruit quality in field pomelo trees. Journal of Agriculture and Food Research 18, 101338.
| Crossref | Google Scholar |

Haiyan G, Lijuan H, Shaoyu L, Chen Z, Ashraf MA (2016) Antimicrobial, antibiofilm and antitumor activities of essential oil of Agastache rugosa from Xinjiang, China. Saudi Journal of Biological Sciences 23(4), 524-530.
| Crossref | Google Scholar | PubMed |

Hatfield JL, Dold C (2019) Water-use efficiency: advances and challenges in a changing climate. Frontiers in Plant Science 10, 103.
| Crossref | Google Scholar | PubMed |

He N, Li Y, Liu C, Xu L, Li M, Zhang J, He J, Tang Z, Han X, Ye Q, Xiao C, Yu Q, Liu S, Sun W, Niu S, Li S, Sack L, Yu G (2020) Plant trait networks: improved resolution of the dimensionality of adaptation. Trends in Ecology & Evolution 35(10), 908-918.
| Crossref | Google Scholar | PubMed |

Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. Journal of Ecology 97(5), 984-991.
| Crossref | Google Scholar |

Hikosaka K, Shigeno A (2009) The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity. Oecologia 160, 443-451.
| Crossref | Google Scholar | PubMed |

Hikosaka K, Yasumura Y, Muller O, Oguchi R (2014) Resource allocation and trade-offs in carbon gain of leaves under changing environment. In ‘Trees in a changing environment: Ecophysiology, adaptation, and future survival’. (Eds M Tausz, N Grulke) pp. 1–24. (Springer Netherlands: Dordrecht)

Hou H-D, Wu C-Y, Zhou J, Xu J-D, Long F, Zhu J-H, Zhou S-S, Zhang W, Mao Q, Shen H, Shi Z-Q, Wei Y-J, Li S-L (2022) Holistic quality evaluation of commercial Agastache rugosa by multiple chromatographic and chemometric analysis. Journal of Pharmaceutical and Biomedical Analysis 210, 114574.
| Crossref | Google Scholar | PubMed |

Hou H-D, Wu C-Y, Zhou J, Long F, Shen H, Xu J-D, Zhou S-S, Mao Q, Wei Y-J, Li S-L (2023) Accumulation patterns of major bioactive components in two chemotypes of Agastache rugosa during flower development evaluated by GC-QQQ-MS/MS and UPLC-QTOF-MS/MS analyses. Industrial Crops and Products 191, 115942.
| Crossref | Google Scholar |

Hyun Choong O, Ji Sook S, Yong Am C (2000) Effect of forms and levels of nitrogen fertilizer on plant growth and essential oil content of Agastache rugosa. Korean Journal of Crop Science 45(2), 128-133.
| Google Scholar |

Kim SW (2020) Korean native wild herbal-based functional ingredient for skin health: Agatri® (Agastache rugosa extract). Food Science and Industry 53, 382-389.
| Google Scholar |

Koistinen J, Sjöblom M, Spilling K (2019) Total nitrogen determination by a spectrophotometric method. In ‘Biofuels from algae: methods and protocols’. (Ed. K Spilling) pp. 81–86. (Springer: New York, NY)

Koistinen J, Sjöblom M, Spilling K (2020) Determining inorganic and organic phosphorus. In ‘Biofuels from algae: methods in molecular biology’. (Ed. K Spilling) pp. 87–94. (New York, NY: Springer)

Lam VP, Kim SJ, Park JS (2020) Optimizing the electrical conductivity of a nutrient solution for plant growth and bioactive compounds of Agastache rugosa in a plant factory. Agronomy 10, 1, 76.
| Crossref | Google Scholar |

Lam VP, Loi DN, Kim S, Shin J, Park J (2023) Ozonated water soaking improves the flower growth, antioxidant activity, and bioactive compound accumulation in Agastache rugosa. Chemical and Biological Technologies in Agriculture 10, 128.
| Crossref | Google Scholar |

Lam VP, Loi DN, Shin J, Mi LK, Park J (2024) Optimization of salicylic acid concentrations for increasing antioxidant enzymes and bioactive compounds of Agastache rugosa in a plant factory. PLoS ONE 19(7), e0306340.
| Crossref | Google Scholar |

Lambers H, Chapin III FS, Pons TL (2019) ‘Plant physiological ecology.’ (Springer Science & Business Media)

Leakey ADB, Ferguson JN, Pignon CP, Wu A, Jin Z, Hammer GL, Lobell DB (2019) Water use efficiency as a constraint and target for improving the resilience and productivity of C3 and C4 Crops. Annual Review of Plant Biology 70, 781-808.
| Crossref | Google Scholar | PubMed |

Lee Y, Lim H-W, Ryu IW, Huang Y-H, Park M, Chi YM, Lim C-J (2020) Anti-inflammatory, barrier-protective, and antiwrinkle properties of Agastache rugosa Kuntze in human epidermal keratinocytes. BioMed Research International 2020, 1759067.
| Crossref | Google Scholar |

Lusk CH, Warton DI (2007) Global meta-analysis shows that relationships of leaf mass per area with species shade tolerance depend on leaf habit and ontogeny. New Phytologist 176(4), 764-774.
| Crossref | Google Scholar | PubMed |

Mills HA, Jones Jr JB (1996) ‘Plant analysis handbook II: a practical sampling, preparation, analysis, and interpretation guide.’ (Micro-Macro Pub: Athens (GA))

Monson RK, Trowbridge AM, Lindroth RL, Lerdau MT (2022) Coordinated resource allocation to plant growth–defense tradeoffs. New Phytologist 233(3), 1051-1066.
| Crossref | Google Scholar | PubMed |

Moore KJ, Dixon PM (2015) Analysis of combined experiments revisited. Agronomy Journal 107(2), 763-771.
| Crossref | Google Scholar |

Motsara MR, Roy RN (2008) ‘Guide to laboratory establishment for plant nutrient analysis.’ (FAO: Rome)

Murchie EH, Ruban AV (2020) Dynamic non-photochemical quenching in plants: from molecular mechanism to productivity. The Plant Journal 101(4), 885-896.
| Crossref | Google Scholar | PubMed |

Okunlola GO, Adelusi AA (2014) Growth and photosynthetic pigment accumulation in Lycopersicum esculentum mill. in response to light and nutrient stress. Notulae Scientia Biologicae 6(2), 250-255.
| Crossref | Google Scholar |

Onoda Y, Wright IJ (2018) The leaf economics spectrum and its underlying physiological and anatomical principles. In ‘The leaf: a platform for performing photosynthesis’. (Eds WW Adams III, I Terashima) pp. 451–471. (Springer International Publishing: Cham)

Park WT, Yeo SK, Sathasivam R, Park JS, Kim JK, Park SU (2020) Influence of light-emitting diodes on phenylpropanoid biosynthetic gene expression and phenylpropanoid accumulation in Agastache rugosa. Applied Biological Chemistry 63, 25.
| Google Scholar |

Pierce S, Maffi D, Faoro F, Cerabolini BEL, Spada A (2022) The leaf anatomical trade-offs associated with plant ecological strategy variation. Plant Ecology 223, 1233-1246.
| Crossref | Google Scholar |

Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193(1), 30-50.
| Crossref | Google Scholar | PubMed |

Poorter H, Niinemets Ü, Ntagkas N, Siebenkäs A, Mäenpää M, Matsubara S, Pons TL (2019) A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytologist 223(3), 1073-1105.
| Crossref | Google Scholar | PubMed |

POWO (2024) Agastache rugosa (Fisch. & C.A.Mey.) Kuntze | plants of the world online | kew science. Available at http://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:444504-1 [accessed August 2023]

Prieto I, León-Sánchez L, Nicolás E, Nortes P, Querejeta JI (2023) Warming reduces both photosynthetic nutrient use efficiency and water use efficiency in Mediterranean shrubsWarming reduces nutrient use efficiency. Environmental and Experimental Botany 210, 105331.
| Crossref | Google Scholar |

Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102(2), 275-301.
| Crossref | Google Scholar |

Rymbai H, Laxman RH, Dinesh MR, Sunoj VSJ, Ravishankar KV, Jha AK (2014) Diversity in leaf morphology and physiological characteristics among mango (Mangifera indica) cultivars popular in different agro-climatic regions of India. Scientia Horticulturae 176, 189-193.
| Crossref | Google Scholar |

Sakuraba Y, Yanagisawa S (2018) Light signalling-induced regulation of nutrient acquisition and utilisation in plants. Seminars in Cell & Developmental Biology 83, 123-132.
| Crossref | Google Scholar | PubMed |

Seemann JR (1989) Light adaptation/acclimation of photosynthesis and the regulation of ribulose-1,5-bisphosphate carboxylase activity in sun and shade plants. Plant Physiology 91(1), 379-386.
| Crossref | Google Scholar | PubMed |

Stitt M, Schulze D (1994) Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant, Cell & Environment 17, 465-487.
| Crossref | Google Scholar |

Valladares F, Laanisto L, Niinemets Ü, Zavala MA (2016) Shedding light on shade: ecological perspectives of understorey plant life. Plant Ecology & Diversity 9(3), 237-251.
| Crossref | Google Scholar |

Vargas M, Glaz B, Alvarado G, Pietragalla J, Morgounov A, Zelenskiy Y, Crossa J (2015) Analysis and interpretation of interactions in agricultural research. Agronomy Journal 107(2), 748-762.
| Crossref | Google Scholar |

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428, 821-827.
| Crossref | Google Scholar | PubMed |

Xiong D, Huang J, Peng S, Li Y (2017) A few enlarged chloroplasts are less efficient in photosynthesis than a large population of small chloroplasts in Arabidopsis thaliana. Scientific Reports 7, 5782.
| Crossref | Google Scholar | PubMed |

Yamani H, Mantri N, Morrison PD, Pang E (2014) Analysis of the volatile organic compounds from leaves, flower spikes, and nectar of Australian grown Agastache rugosa. BMC Complementary and Alternative Medicine 14, 495.
| Crossref | Google Scholar | PubMed |

You C, Wu F, Yang W, Xu Z, Tan B, Zhang L, Yue K, Ni X, Li H, Chang C, Fu C (2018) Does foliar nutrient resorption regulate the coupled relationship between nitrogen and phosphorus in plant leaves in response to nitrogen deposition? Science of the Total Environment 645, 733-742.
| Crossref | Google Scholar | PubMed |

Yuan ZY, Chen HYH (2015) Negative effects of fertilization on plant nutrient resorption. Ecology 96(2), 373-380.
| Crossref | Google Scholar | PubMed |