Complex trait relationships between leaves and absorptive roots: Coordination in tissue N concentration but divergence in morphology

Abstract Leaves and absorptive roots (i.e., first‐order root) are above‐ and belowground plant organs related to resource acquisition; however, it is controversy over whether these two sets of functional traits vary in a coordinated manner. Here, we examined the relationships between analogous above‐ and belowground traits, including chemical (tissue C and N concentrations) and morphological traits (thickness and diameter, specific leaf area and root length, and tissue density) of 154 species sampling from eight subtropical and temperate forests. Our results showed that N concentrations of leaves and absorptive roots were positively correlated independent of phylogeny and plant growth forms, whereas morphological traits between above‐ and belowground organs varied independently. These results indicate that, different from plant economics spectrum theory, there is a complex integration of diverse adaptive strategies of plant species to above‐ and belowground environments, with convergent adaptation in nutrient traits but divergence in morphological traits across plant organs. Our results offer a new perspective for understanding the resource capture strategies of plants in adaptation to heterogeneous environments, and stress the importance of phylogenetic consideration in the discussion of cross‐species trait relationships.

[1]  G. Mohren,et al.  Towards a multidimensional root trait framework: a tree root review. , 2016, The New phytologist.

[2]  S. Arndt,et al.  Life span and structure of ephemeral root modules of different functional groups from a desert system. , 2016, The New phytologist.

[3]  A. Stokes,et al.  Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. , 2016, The New phytologist.

[4]  Guirui Yu,et al.  Coordinated pattern of multi-element variability in leaves and roots across Chinese forest biomes , 2016 .

[5]  C. Blackwood,et al.  Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms , 2016, Plant and Soil.

[6]  H. Zeng,et al.  Economic strategies of plant absorptive roots vary with root diameter , 2016 .

[7]  Fanglan Li,et al.  New insights into leaf and fine‐root trait relationships: implications of resource acquisition among 23 xerophytic woody species , 2015, Ecology and evolution.

[8]  Guirui Yu,et al.  Latitudinal variation of leaf stomatal traits from species to community level in forests: linkage with ecosystem productivity , 2015, Scientific Reports.

[9]  Q. Zhang,et al.  Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. , 2015, Ecology letters.

[10]  Dali Guo,et al.  Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. , 2015, The New phytologist.

[11]  C. Blackwood,et al.  Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees , 2015 .

[12]  J. Gutiérrez,et al.  Resource economics and coordination among above- and below-ground functional traits of three dominant shrubs from the Chilean coastal desert. , 2015 .

[13]  L. Mommer,et al.  Going underground: root traits as drivers of ecosystem processes. , 2014, Trends in ecology & evolution.

[14]  H. Zeng,et al.  Leading dimensions in absorptive root trait variation across 96 subtropical forest species. , 2014, The New phytologist.

[15]  Jinsheng He,et al.  Alpine climate alters the relationships between leaf and root morphological traits but not chemical traits , 2014, Oecologia.

[16]  P. Reich.  The world‐wide ‘fast–slow’ plant economics spectrum: a traits manifesto , 2014 .

[17]  Daniel C. Laughlin,et al.  The intrinsic dimensionality of plant traits and its relevance to community assembly , 2014 .

[18]  H. Zeng,et al.  Variation of first‐order root traits across climatic gradients and evolutionary trends in geological time , 2013 .

[19]  P. Cruz,et al.  Root and leaf functional trait relations in Poaceae species: implications of differing resource-acquisition strategies , 2013 .

[20]  D. Wardle,et al.  Plasticity in above- and belowground resource acquisition traits in response to single and multiple environmental factors in three tree species , 2013, Ecology and Evolution.

[21]  L. Mommer,et al.  The role of roots in the resource economics spectrum. , 2012, The New phytologist.

[22]  T. Jombart,et al.  How to measure and test phylogenetic signal , 2012 .

[23]  D. Coomes,et al.  Species‐ and community‐level patterns in fine root traits along a 120 000‐year soil chronosequence in temperate rain forest , 2011 .

[24]  J. Cahill,et al.  Independent Evolution of Leaf and Root Traits within and among Temperate Grassland Plant Communities , 2011, PloS one.

[25]  Liam J. Revell,et al.  Phylogenetic signal and linear regression on species data , 2010 .

[26]  J. Cornelissen,et al.  Coordinated variation in leaf and root traits across multiple spatial scales in Chinese semi-arid and arid ecosystems. , 2010, The New phytologist.

[27]  J. Cornelissen,et al.  Evidence of the ‘plant economics spectrum’ in a subarctic flora , 2010 .

[28]  Liam J. Revell,et al.  Size-Correction and Principal Components for Interspecific Comparative Studies , 2009, Evolution; international journal of organic evolution.

[29]  L. Comas,et al.  Patterns in root trait variation among 25 co-existing North American forest species. , 2009, The New phytologist.

[30]  L. Poorter,et al.  Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. , 2009, The New phytologist.

[31]  Y. Liu,et al.  Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. , 2008, The New phytologist.

[32]  Campbell O. Webb,et al.  Bioinformatics Applications Note Phylocom: Software for the Analysis of Phylogenetic Community Structure and Trait Evolution , 2022 .

[33]  Barbara R. Holland,et al.  Analysis of Phylogenetics and Evolution with R , 2007 .

[34]  C. Violle,et al.  Let the concept of trait be functional , 2007 .

[35]  William F. Fagan,et al.  Phylogenetic and Growth Form Variation in the Scaling of Nitrogen and Phosphorus in the Seed Plants , 2006, The American Naturalist.

[36]  P. Reich,et al.  COMPARISONS OF STRUCTURE AND LIFE SPAN IN ROOTS AND LEAVES AMONG TEMPERATE TREES , 2006 .

[37]  Mark Westoby,et al.  Land-plant ecology on the basis of functional traits. , 2006, Trends in ecology & evolution.

[38]  P. Reich,et al.  Linking leaf and root trait syndromes among 39 grassland and savannah species. , 2005, The New phytologist.

[39]  Joseph M. Craine,et al.  ENVIRONMENTAL CONSTRAINTS ON A GLOBAL RELATIONSHIP AMONG LEAF AND ROOT TRAITS OF GRASSES , 2005 .

[40]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[41]  P. Reich,et al.  A handbook of protocols for standardised and easy measurement of plant functional traits worldwide , 2003 .

[42]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[43]  T. Garland,et al.  Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods , 2002 .

[44]  Michael F. Allen,et al.  FINE ROOT ARCHITECTURE OF NINE NORTH AMERICAN TREES , 2002 .

[45]  Mark W. Chase,et al.  Evolution of the angiosperms: calibrating the family tree , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  M. Pagel.  Inferring the historical patterns of biological evolution , 1999, Nature.