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Phenotypic plasticity and integration synergistically enhance plant adaptability to flooding and nitrogen stresses

February 2025
Plant and Soil

Authors:

中国科学院大学

Aims Plants respond to stress gradients by modifying various aspects of their morphology, physiology, architecture, allocation and mycorrhizal fungi. Yet, understanding how plants adapt to resource stress requires a comprehensive, integrated perspective that considers not only the consistency and variability of individual trait adjustments, but also the interplay between two key mechanisms: phenotypic plasticity (the direction and magnitude of trait adjustment) and phenotypic integration (the degree and pattern of trait covariation). Despite their importance, the coordination of these mechanisms in driving adaptive responses remains poorly understood. Methods To address these gaps, we measured the adjustment of 27 above- and below-ground traits across three dominant species (Cynodon dactylon, Xanthium strumarium, and Bidens tripartita), and explored trait networks, and the relationship between phenotypic plasticity and phenotypic integration in response to flooding and/or nitrogen in riparian habitats on the Three Gorges Reservoir area, China. Results The results show that both flooding and nitrogen stress induced shifts in species traits towards more acquisitive strategy, characterized by larger leaves, higher leaf nutrient concentrations, finer roots, larger specific root lengths, greater branching intensity, and elevated carboxylate concentrations. Flooding altered the hub trait with the highest centrality in the trait network from root branching intensity to leaf phosphorus content, while nitrogen stress shifted the hub trait from leaf area to root phosphorus content. Furthermore, a positive correlation was observed between phenotypic plasticity and integration, indicating that higher plasticity of functional traits facilitated better integration with other traits under flooding and nitrogen stress. Conclusions These findings suggest that plants exhibit more acquisitive traits in habitats experiencing flooding and/or nitrogen stress. Furthermore, a comprehensive assessment of phenotypic plasticity and its integration under compound stresses underscores the critical role of synergies between plasticity and integration in enhancing plant adaptability to environmental changes.

Overview of the dominant species characteristics considered in this study in response to flooding and nutrient stress. Leaf morphology traits included leaf area (LA), specific leaf area (SLA), leaf dry matter content (LDMC); leaf physiology traits included peroxidase (POD), catalase (CAT), superoxide dismutase (SOD), malondialdehyde (MDA), hydrogen peroxide (H2O2), proline (Pro), soluble protein (SP), soluble sugar (SS); Leaf chemical traits including leaf carbon content (LCC), leaf nitrogen content (LNC); leaf phosphorus content (LPC); Leaf allocation traits include leaf mass fraction (LMF). Root morphology traits included root diameter (RD), root tissue density (RTD), root dry matter content (RDMC), root length (RL), specific root length (SRL); Root architectural traits included root branching intensity (RB); Root mycorrhizal colonization included AMF colonization rates; Root physiological traits including carboxylates (CAR); Root chemical traits including root carbon content (RCC), root nitrogen content (RNC), root phosphorus content (RPC); Root allocation traits include root mass fraction (RMF)

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Direction and magnitude of plasticity adjustments in response to resource stress. Phenotypic plasticity, quantified on a scale from 0 to 1, reflects the extent of this adjustment, where 0 denotes no plasticity and 1 indicates maximum plasticity. Notably, negative values observed in the experiment signify the direction of trait adjustment rather than challenging the established range of phenotypic plasticity. Significance of the trait adjustments as taken from Tables S3 and S4 (*, P < 0.05; **, P < 0.01; ***, P < 0.001; ns, nonsignificant)

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Cross-species trait networks and ‘Betweenness’ of nodes in response to flooding (top) and nitrogen stress (bottom). Fig. a (flooding), b (non-flooded) show the trait networks under flooding stress, and fig. c (flooding stress) shows the ‘Betweenness’ of nodes; Fig. d (nitrogen sufficiency), e (nitrogen limitation) show the trait networks under nitrogen stress, and Fig. f shows the ‘Betweenness’ of nodes under nitrogen stress. Green and orange colours indicate non-flooded and flooding treatments, respectively; red and blue colours indicate nitrogen limitation and nitrogen sufficiency treatments, respectively. Solid and dashed lines indicate positive and negative correlations, respectively. Only significant correlations (P < 0.05) are shown, and the strength of the correlation is indicated by the thickness of the edges. Bold red parts of the network show the highest values of ‘Betweenness’ (i.e. the number of shortest paths from all nodes to all other nodes through a focal node). Green, red, orange, purple and blue circles indicate plant morphological, architectural, physiological, chemical and mycorrhizal fungal colonisation, respectively

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Changes in plant phenotypic plasticity (magnitude and direction of trait adjustment to resource stress). a Above-ground trait adjustment to flooding stress; b Below-ground trait adjustment to nitrogen stress. The heterogeneity of species’ responses to resource stress is assessed via the strength (F) and significance (P < 0.05) of the species × stress interaction factors of three-way ANOVAs. Standard errors represent: a the variation between species adjustments to flooding stress in nitrogen limitation vs nitrogen sufficiency conditions; b the variation between species adjustments to nitrogen stress in flooding vs non-flooded conditions

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Above- and below-ground phenotypic plasticity cross species a: the negative sign preceding the phenotypic plasticity value indicates solely the direction of functional trait adjustment. Phenotypic integration b: the colours of the ellipses indicate covariance coefficients, with red indicating positive covariance and blue indicating negative covariance; the darker the colour, the greater the absolute value of the covariance coefficient. Regression analysis of phenotypic plasticity and phenotypic integration c: the shaded area in each panel indicates the 95% confidence interval of the fit test. *P < 0.05

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Plant Soil

https://doi.org/10.1007/s11104-025-07230-y

RESEARCH ARTICLE

Phenotypic plasticity andintegration synergistically

enhance plant adaptability toﬂooding andnitrogen stresses

JunYang· ZhenxingZhou· WanyuQi·

XianleiGao· YueWang· XiangtaoWang·

XuemeiYi· MaohuaMa · ShengjunWu

Received: 12 October 2024 / Accepted: 12 January 2025

Abstract

Aims Plants respond to stress gradients by modify-

ing various aspects of their morphology, physiology,

architecture, allocation and mycorrhizal fungi. Yet,

understanding how plants adapt to resource stress

requires a comprehensive, integrated perspective that

considers not only the consistency and variability of

individual trait adjustments, but also the interplay

between two key mechanisms: phenotypic plastic-

ity (the direction and magnitude of trait adjustment)

and phenotypic integration (the degree and pattern

of trait covariation). Despite their importance, the

coordination of these mechanisms in driving adaptive

responses remains poorly understood.

Methods To address these gaps, we measured the

adjustment of 27 above- and below-ground traits

across three dominant species (Cynodon dactylon,

Xanthium strumarium, and Bidens tripartita), and

explored trait networks, and the relationship between

phenotypic plasticity and phenotypic integration in

response to ﬂooding and/or nitrogen in riparian habi-

tats on the Three Gorges Reservoir area, China.

Results The results show that both ﬂooding and nitro-

gen stress induced shifts in species traits towards more

acquisitive strategy, characterized by larger leaves,

higher leaf nutrient concentrations, ﬁner roots, larger

speciﬁc root lengths, greater branching intensity, and

elevated carboxylate concentrations. Flooding altered

the hub trait with the highest centrality in the trait net-

work from root branching intensity to leaf phosphorus

content, while nitrogen stress shifted the hub trait from

leaf area to root phosphorus content. Furthermore, a

positive correlation was observed between phenotypic

Responsible Editor: Al Imran Malik.

Supplementary Information The online version

contains supplementary material available at https:// doi.

org/ 10. 1007/ s11104- 025- 07230-y.

J.Yang· Z.Zhou· W.Qi· X.Yi· M.Ma(*)·

S.Wu(*)

CAS Key Laboratory ofReservoir Aquatic Environment,

Chongqing Institute ofGreen andIntelligent Technology,

Chinese Academy ofSciences, Chongqing400713, China

e-mail: mamaohua@cigit.ac.cn

S. Wu

e-mail: wsj@cigit.ac.cn

J.Yang

Chongqing School, University ofChinese Academy

ofSciences (UCAS Chongqing), Chongqing400713,

China

X.Gao

Faculty ofScience, Tibet University, Lhasa850000, China

Y.Wang

CAS Key Laboratory ofMountain Ecological Restoration

andBioresource Utilization & Ecological Restoration

andBiodiversity Conservation Key Laboratory ofSichuan

Province, Chengdu Institute ofBiology, Chinese Academy

ofSciences, Chengdu610042, China

X.Wang

School ofLife Sciences, Guizhou Normal University,

Guiyang550025, China

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

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Phenotypic plasticity and integration synergistically enhance plant adaptability to flooding and nitrogen stresses

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