The worldwide leaf economic spectrum traits are closely linked with mycorrhizal traits
Introduction
The traits of green leaves play key roles in plant physiological processes such as photosynthesis, respiration and transpiration, and in biological and economic productivity of plants. Leaf economic spectrum (LES), first proposed by Wright et al. (2004), consisted of six key fundamental traits: leaf lifespan (LL), leaf mass per area (LMA), photosynthetic capacity (Amass), leaf N concentration (Nmass), leaf P concentration (Pmass), and dark respiration rate (Rmass). LES analysis provides quantitative results of plant functional traits and their relationships at regional or global scales, and helps to understand leaf investment strategies of different plant groups. LES may play large roles in ecosystem processes and functions, such as water utilization, nutrient cycling, primary productivity, and decomposition (Bill et al., 2006; Reich, 2014). Thus, LES has aroused increasing interest (Donovan et al., 2011; Osnas et al., 2013; Onoda et al., 2017; Anderegg et al., 2018), particularly, the relationship between mycorrhizal status and plant economic spectrum (Reich, 2014; Jespersen et al., 2019).
The morphology, chemical composition and physiological characteristics of leaves are interrelated and interdependent. Direct and indirect causal relationships often exist between leaf economic traits. Previous findings have shown that the LES traits co-vary tightly across all plant species (Wright et al., 2004; Osnas et al., 2013; Read et al., 2014). For instance, there is a direct causal relationship between high Amass and high Nmass (Wright et al., 2004). The close relationships among LES traits suggest a strategy of allocating limited available resources among plant functional traits to support their growth and development, and plants can modulate the interrelationships and thus balance their fitness such as survival, growth and reproduction (Navas et al., 2010; Whitman and Aarssen, 2010). However, whether the correlations among LES traits vary with root mycorrhizal status remains unknown.
There is increasing recognition that LES traits are biological characteristics that the plants adapt to external environments (Dı́az and Cabido, 2001; Reich et al., 2003). Numerous studies have found that LES traits are influenced by plant characteristics and the environments, such as plant species and community, climate, altitude, and soil properties (Roche et al., 2004; Asner et al., 2016; Riva et al., 2016; Anderegg et al., 2018). However, the findings are sometimes contradictory. Some studies found that climate weakly or modestly modulated leaf traits (Wright et al., 2004; He et al., 2010). However, another study found significant climatic and geophysical controls on LES traits and their interrelationships (Asner et al., 2016). Actually, both natural selection and genetic variation influence leaf traits, but natural selection probably poses the most significant influence in the evolution of the worldwide LES (Donovan et al., 2011). However, the responses of LES traits and their interrelationships to biotic factors such as mycorrhizal features still need to be addressed.
Mycorrhizal status of plants is among the most typical belowground traits, as most terrestrial plants can form mycorrhizal symbioses (van der Heijden et al., 2015). Plants with thick roots generally form mycorrhizal symbioses which help them acquire soil resources, allowing plants to colonize new challenging habitats in their evolution (Ma et al., 2018). Mycorrhizal features can be considered as part of the root economic spectrum constituting the whole plant economic spectrum, and produce direct and indirect impacts on LES (Reich, 2014). As one of the most abundant symbiotic associations in nature, arbuscular mycorrhizas (AMs) co-evolved with plants since their first colonization on land about 450–500 million years ago (Cairney, 2000). AMs facilitate host plants to take up mineral nutrients in exchange for photosynthate (Smith and Read, 2008), benefit plants at both individual and community levels, and further affect ecosystem processes and functioning (van der Heijden et al., 1998; Rillig, 2004; van der Heijden and Scheublin, 2007). The most well-known benefit from arbuscular mycorrhizal (AM) fungi (AMF) is to improve the nutritional status of host plants, including P and N (Smith and Smith, 2011). AMF also improve plant photosynthesis and respiration rates via increased nutrient uptake and carbon sink stimulation (Kaschuk et al., 2009; Shi et al., 2018). Undoubtedly, LES traits and relations with mycorrhizal strategy are of significance for plant fitness (Wright et al., 2004), deserving more recognition.
A few studies have focused on economic traits of plants with different mycorrhizal types including AMs, but no definitive conclusion can be drawn, probably due to variations in phylogeny, growth form, and habitat. Valverde-Barrantes et al. (2017) found mycorrhizal types had little impact on roots traits. Koele et al. (2012) found no consistent impact of ectomycorrhizas on LES traits. At the community level, leaf traits covary with AM features during plant succession (Jespersen et al., 2019). AM leaf litters decayed faster than ectomycorrhizal litters in temperate forests, which can be explained by litter N and phylogeny (Keller and Phillips, 2019). Our previous study found that AMs significantly affected the leaf traits Nmass and Amass of the 54 plant species on the Tibetan Plateau, and mycorrhizal response varied with precipitation and temperature (Shi et al., 2012). However, the relationship between AMs and the global LES traits remains unknown.
In the present study, the worldwide LES traits of AM and nonAM plants were compared, and the interrelationships among the LES traits were analyzed. Our aims are to test whether plants with or without AM associations have different LES traits at the global scale, and to understand the investment-return strategy for plants to cope with the environments.
Section snippets
Data compilation
In this study, the global leaf trait data were obtained from the database established by Wright et al. (2004). On this basis, we established a new database including leaf characteristics and mycorrhizal type according to the mycorrhizal types of plants. The mycorrhizal type of each plant species was ascertained according to the published literature, especially Harley and Harleye (1990), Wang and Qiu (2006), Koele et al. (2012), and Shi et al. (2017). We classified all the plants with typical AM
LES traits of AM and nonAM plants
All the six LES traits varied greatly for both AM and nonAM plants, but the ranges were much larger for AM plants (Fig. 1). LL ranged from 0.94 to 288 months for AM plants, while from 1.35 to 240 months for nonAM plants. LMA ranged from 14.4 to 781.3 g m−2 and from 16.4 to 454.5 g m−2 for AM and nonAM plants respectively; Nmass from 0.334% to 6.36% and from 0.62% to 5.62% respectively; Pmass from 0.018% to 0.6% and from 0.01% to 0.37% respectively; Amass from 11.6 to 662.25 nmol g−1 s−1 and
Discussion
Here we first evaluated the relationship between AM strategy and the global LES traits, and found significant differences in the six LES traits except Pmass between AM and nonAM plants. It has been widely recognized that AMs play important roles in plants' mineral nutrient acquisition (George et al., 1995; Smith et al., 2011; Hodge and Storer, 2015), and plants’ tolerance to stressful environments (Miransari, 2010; Wang, 2017; Wang et al., 2019). AM plants generally exhibit better performance
Author contributions
ZS and FW designed the research; KL, FW, and XZ undertook data analysis and interpretation, and contributed to writing the manuscript.
Acknowledgements
We thank Dr. X. Jing for his kind help on data analysis. This work was supported by the National Natural Science Foundation of China (31670499, 41471395), the Program for Science & Technology Innovation Talents in Universities of Henan Province (18HASTIT013), the Doctoral Foundation of QUST (0100229003), Key Laboratory of Mountain Surface Processes and Ecological Regulation, CAS (20160618), Laboratory for Earth Surface Processes, Ministry of Education (201612), the Innovation Team Foundation of
References (50)
The advantages of being evergreen
Trends Ecol. Evol.
(1995)- et al.
Non-mycorrhizal plants: the exceptions that prove the rule
Trends Plant Sci.
(2018) - et al.
Vive la différence: plant functional diversity matters to ecosystem processes
Trends Ecol. Evol.
(2001) - et al.
The evolution of the worldwide leaf economics spectrum
Trends Ecol. Evol.
(2011) - et al.
Mycorrhizal features and leaf traits covary at the community level during primary succession
Fungal Ecol.
(2019) - et al.
Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses?
Soil Biol. Biochem.
(2009) - et al.
Variations in leaf functional traits among plant species grouped by growth and leaf types in Zhenjiang, China
J. For. Res.
(2017) Nutrient resorption from senescing leaves of perennials - are there general patterns?
J. Ecol.
(1996)- et al.
Within-species patterns challenge our understanding of the leaf economics spectrum
Ecol. Lett.
(2018) - et al.
Large-scale climatic and geophysical controls on the leaf economics spectrum
Proc. Natl. Acad. Sci. U.S.A.
(2016)