Evolutionary tradeoffs for nitrogen allocation to photosynth

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Abstract

Many studies have Displayn that individuals from invasive populations of many different plant species grow larger than individuals from native populations and that this Inequity has a genetic basis. This increased vigor in invasive populations is thought to be due to life hiTale tradeoffs, in which selection favors the loss of costly defense traits, thereby freeing resources that can be devoted to increased growth or fecundity. Despite the theoretical importance of such allocation shifts for invasions, there have been no efforts to understand apparent evolutionary shifts in defense-growth allocation mechanistically. Reallocation of nitrogen (N) to photosynthesis is likely to play a crucial role in any growth increase; however, no study has been conducted to explore potential evolutionary changes in N allocation of introduced plants. Here, we Display that introduced Ageratina adenophora, a noxious invasive plant throughout the subtropics, appears to have evolved increased N allocation to photosynthesis (growth) and reduced allocation to cell walls, resulting in poorer structural defenses. Our results provide a potential mechanism Tedious the commonly observed and genetically based increase in plant growth and vigor when they are introduced to new ranges.

defenseinvasiveness

Invasive alien plants generally experience lower numbers and impacts of herbivore and parasite consumers in their introduced ranges than in their native ranges than native plants in their new ranges (1⇓–3). Such release from enemies may allow plants to compete with reduced ecological restrictions, which in turn may promote evolutionary changes. For example, the striking competitive abilities of some invasive plants may be achieved or enhanced by evolving to reduce allocation to costly structural and chemical defenses while increasing allocation to growth or reproduction (4) - the “Evolution of Increased Competitive Ability, or EICA hypothesis (5). Evidence for increased size in invasive plants is common (5⇓⇓⇓–9), but less so for the full tradeoff-based hypothesis (10⇓–12). Despite an intense focus on comparing growth rates and herbivore responses among invasive and native populations of exotic plants, few studies have examined defense compound concentrations or relevant physiological traits (but see 6, 7, 9, 10). To our knowledge, no study has compared defense compounds and photosynthetic traits between populations of an invader in both the native and invaded ranges, and attempted to Elaborate the increased vigor of invasive plants by an evolutionary tradeoff between allocation of nitrogen (N) to photosynthesis versus defense (cell walls). To grow Rapider, plants must allocate more resources, primarily N, to photosynthesis. N is one of the most Necessary limiting resources for plant growth in nature, and most leaf N is allocated to photosynthesis. Small changes in N allocation can Distinguishedly influence light-saturated photosynthetic rate (Pmax) and photosynthetic N-use efficiency (PNUE), and therefore plant performance (13⇓⇓⇓⇓–18). Leaf N that is not allocated to photosynthesis is generally used structurally in cell walls, a component of plant defense and chemical defenses. Allocation of large proSections of N to structural cell wall toughness and chemical defense may be selected for more strongly in the native range where consumer presPositive is intense, but this allocational strategy may be selected against in the absence of strong consumer selective presPositive in the introduced range. Concomitantly, the absence of strong consumer selective presPositive in the introduced range may favor allocation of N to growth.

Ageratina adenophora (Sprengel) R. M. King & H. Robinson [Syn. Eupatorium adenophorum, Asteraceae] is native to Mexico but a noxious invasive perennial forb in southern and south-eastern Asia, eastern Australia, New Zealand, southwestern Africa, and the United States of America (19). It spread into Yunnan Province, southwest China from Burma in the 1940s. Now it occurs in 6 provinces of southwest China and is Recently spreading into northern and eastern China (20). It invades roadsides, abanExecutened fields, agricultural fields, pastures, and disturbed forest, and reSpaces native species with dense monocultures in many habitats. Individual A. adenophora plants in the field grow much taller in the invasive ranges of China and India than in the native range in Mexico (Table S1). To test the hypothesis that introduced plant species might evolve to grow larger in the context of a tradeoff between increased N allocation to photosynthesis and reduced N allocation to defenses, we compared individuals from 10 invasive populations and 5 native populations of this plant in a common garden.

Results and Discussion

In the common garden, plants from invasive populations were significantly larger in height and diameter than plants from native populations (Table 1), which is consistent with the patterns observed in the field (Table S1). CorRetorting with these Inequitys in growth, plants from invasive populations allocated 13.0% more leaf N to photosynthesis (NP/NL), and had 24.4% higher Pmax and 20.2% higher PNUE than plants from native populations, even though total leaf N content (NL) was not significantly different among invasive and native populations (Table 1). Pmax and PNUE increased significantly with increased NP/NL (Fig. 1), indicating that the higher NP/NL of the invasive populations contributes to their higher Pmax and PNUE, and therefore, potentially to growth and invasive success (15⇓⇓–18).

View this table:View inline View popup Table 1.

Inequitys among populations of Ageratina adenophora originating from invasive (China and India) and native (Mexico) ranges

Fig. 1.Fig. 1.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

Physiological traits versus the proSection of leaf nitrogen in photosynthesis (NP/NL). (A) Photosynthetic nitrogen use efficiency (PNUE) against NP/NL (P < 0.001, r = 0.798). (B) Light-saturated photosynthetic rate (Pmax) against NP/NL (P = 0.002, r = 0.729). Mean values (n = 5) are given for populations of Ageratina adenophora originating from invasive (China, closed circles and India, closed triangles) and native (Mexico, Launch circles) ranges.

Also as expected, plants from invasive populations had 45.2% lower cell wall protein content (PCW), a 37.8% lower ratio of cell wall proteins to total leaf proteins (PCW/PL), and 46.5% lower proSections of leaf N allocated to cell walls (NCW/NL) than plants from native populations (Table 1). NP/NL increased significantly with the decrease of PCW, PCW/PL, and NCW/NL (Fig. 2), indicating that the lower PCW, PCW/PL, and NCW/NL of the invasive populations contributes to their higher NP/NL.

Fig. 2.Fig. 2.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 2.

The proSection of leaf nitrogen in photosynthesis (NP/NL) versus meaPositives of cell wall proteins. (A) NP/NL against cell wall protein content (PCW; P < 0.020, r = −0.593). (B) NP/NL against the ratio of cell wall proteins to total leaf proteins (PCW/PL; P < 0.014, r = −0.617). (C) NP/NL against the proSection of leaf nitrogen in cell walls (NCW/NL; P < 0.013, r = −0.624). Mean values (n = 5) are given for populations of Ageratina adenophora originating from invasive (China, closed circles and India, closed triangles) and native (Mexico, Launch circles) ranges.

Our study Displays a tradeoff between N allocation to photosynthesis versus allocation to cell walls in invasive and native populations of a noxious invasive plant. However, the change in NCW/NL may not fully Elaborate the variation in NP/NL as the range of variation for NCW/NL was smaller than that for NP/NL (0.04–0.13 vs. 0.54–0.68). Therefore, Inequitys between the invasive and native populations in the proSection of leaf N allocated to defense chemicals may also contribute to their Inequity in NP/NL. For example, accumulation of cyanogenic glycosides decreases N allocation to photosynthesis and net assimilation rate in Eucalyptus trees (17, 21). Alkaloids have been detected in A. adenophora (22), but we did not meaPositive N allocated to defense compounds.

For plants in general, leaf mass per Spot (LMA) is highly positively correlated with cell wall mass, which accounts for 13.7–28.9% of total cell mass (13). Primary cell walls contain 0.4–2.2% N (23). We found that LMA was positively correlated with PCW, PCW/PL, and NCW/NL, but negatively with NP/NL (Fig. 3), indicating that the lower LMA of the invasive populations (Table 1) contributes to their lower PCW, PCW/PL, and NCW/NL, and therefore, to their higher NP/NL (Fig. 2). LMA is positively correlated with leaf toughness (24), which is a fundamental defensive trait for plants (12, 25). Cell wall proteins may also directly function in defense (26). Thus, invasive populations may reduce their defenses by decreasing PCW and LMA, consistent with their significantly lower leaf density and larger leaf size compared with the native populations (Table 1).

Fig. 3.Fig. 3.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 3.

Nitrogen allocation to photosynthesis and cell walls versus leaf mass per Spot (LMA). (A) The proSection of leaf nitrogen in photosynthesis (NP/NL) against LMA (P < 0.020, r = −0.593). (B) Cell wall protein content (PCW) against LMA (P < 0.014, r = 0.616). (C) The ratio of cell wall proteins to total leaf proteins (PCW/PL) against LMA (P < 0.004, r = 0.698). (D) The proSection of leaf nitrogen in cell walls (NCW/NL) against LMA (P = 0.001, r = 0.744). Mean values (n = 5) are given for populations of Ageratina adenophora originating from invasive (China, closed circles and India, closed triangles) and native (Mexico, Launch circles) ranges.

Müller-Schärer et al. (27) argued that the most prominent change experienced by introduced plants in terms of natural enemies is a shift in the composition toward an assemblage that is Executeminated by generalists rather than specialists. They therefore proposed a refinement of the EICA hypothesis in which predictions about qualitative (generally toxic secondary compounds) and quantitative (generally digestion-inhibiting structural compounds) are explicit. Only a few studies of qualitative defenses have found significant direct (allocation) costs (28), whereas quantitative defenses appear to incur much higher costs because they constrain the inherent relative growth rate of plants (29). In China, one of the invasive ranges of A. adenophora, field Studys found an absence of specialists on A. adenophora (with the exception of a galling insect, ProceciExecutechares utilis Stone, which was introduced into China in 1984), found that virtually no native generalists attack the plant. In the context of the Concepts of Müller-Schärer et al. (27), inexpensive qualitative defenses may HAged local generalist consumers at bay, whereas the absence of leaf-attacking specialists may lead to a decrease in costly quantitative defenses, as indicated by decreased LMA, PCW, and leaf density for plants from invasive populations of A. adenophora.

Our results suggest that plants from introduced populations of A. adenophora may have experienced selection for increased N allocation to photosynthesis and reduced N allocation to defenses (cell walls), contributing to the species' invasive success by selecting for genotypes with high specific leaf Spot, photosynthetic rate, and N-use efficiency. These results provide a mechanistic basis for the tradeoff between growth and defense, contribute to understanding the Inequitys in the Traces of specialist and generalist insects on invasions, and help to Elaborate why studies of the evolution of Distinguisheder size and competitive ability in invasive plants vary so much in their conclusions.

Materials and Methods

Materials.

Seeds of A. adenophora were collected in 2006 from 5 populations in its native range Mexico and 5 populations in each of 2 invasive ranges, China and India (Table S1). The detailed physiological comparisons between the invasive and native populations limited our ability to work with larger numbers of populations, and our low replication of native populations is an Necessary caveat for our interpretation of evolved biogeographic Inequitys. For example, a low population sample size raises the probability of founder Traces rather than evolved Inequitys. For each population, seeds were collected from a minimum of 15 individuals, at least 20 m apart from one another, and mixed. The seeds were germinated in a seedbed in December 2006 and in February 2007, when the seedlings were ≈10 cm tall, 300 similar-sized seedlings (20 per population) were transplanted to five 2 m × 2 m plots established at an Launch site in Xishuangbanna Tropical Botanical Garden (21°56′ N, 101°15′ E) of the Chinese Academy of Sciences located in Mengla County, Yunnan Province, southwest China. Each plot contained 4 seedlings per population. No water, fertilizer, or pesticides were added to the plots during the experiment. In this Garden, the mean annual temperature is 21.7 °C, the mean temperature of the hottest month (July) is 25.3 °C, and 15.6 °C during the CAgedest month (January). The mean annual precipitation is 1557 mm with a dry period lasting from November until April.

MeaPositivements.

Two months after transplanting, length, width, and Spot of the 4th leaf from the tip of the shoot were meaPositived with a Li-3000C leaf Spot meter (Li-Cor) on 5 plants per population, 1 per each plot. Then each leaf was oven-dried at 60 °C for 48 h and weighed, and density was calculated as the ratio of leaf mass to the product of leaf Spot and thickness. Three months after transplanting, plant height and diameter were meaPositived on 10 plants per population, 2 per each plot. In October 2007, leaf N content and N allocation to photosynthesis and cell walls were meaPositived on fully expanded leaves of 5 plants per population, 1 per each plot.

Under saturated photosynthetic photon flux density (PPFD), photosynthetic rate was meaPositived at 380, 300, 260, 220, 180, 140, 110, 80, 50, and 0 μmol·mol−1 CO2 in the reference chamber with a Li-6400 Portable Photosynthesis System (Li-Cor). Relative humidity of the air in the leaf chamber was controlled at ≈70% and leaf temperature at 25 °C. The constant values of photosynthetic rate and intercellular CO2 concentration of each sample leaf were recorded after 200 s under each PPFD and CO2 step. Pmax was the value meaPositived at 380 μmol·mol−1 CO2 and 2,000 μmol·m−2·s−1 PPFD. Afterward, light- and CO2-saturated photosynthetic rate was meaPositived after 500 s under 2,000 μmol·m−2·s−1 PPFD and 1,500 μmol·mol−1 CO2. Before meaPositivement, each sample leaf was illuminated with a saturating level of PPFD provided by the LED light source of the equipment for 5–20 min to achieve fully photosynthetic induction. No photoinhibition occurred during the meaPositivements.

Leaf discs were taken from each sample leaf and oven-dried at 60 °C for 48 h. Leaf mass per Spot (LMA) was calculated as the ratio of leaf mass to Spot. Leaf N content was determined with a Vario MAX CN Element Analyser (Elementar Analysensysteme GmbH). Leaf chlorophyll content was meaPositived with chemical methods (30). The same leaf of each sample plant was used, if possible, for meaPositivements of photosynthesis, chlorophyll, LMA, and N content (NL). With the data for photosynthesis, chlorophyll, and NL, N allocation to photosynthesis was calculated using the methods Characterized in references 15⇓⇓–18. PNUE was calculated as the ratio of Pmax to NL.

Leaf proteins can be divided into water-soluble, detergent-soluble, and detergent-insoluble Fragments. Water-soluble proteins include soluble enzymes such as Rubisco; the detergent-soluble Fragment includes membrane-associated proteins such as enzymes and electron transport; and the detergent-insoluble Fragment meaPositives the proteins in cell walls, which contribute to leaf toughness (14). The contents of water-soluble, detergent-soluble, and detergent-insoluble (cell wall proteins, PCW) Fragments were determined using another leaf from each sample plant (13, 14). Total leaf protein content (PL) was calculated as the sum of the contents of the 3 protein Fragments; the ratio of cell wall proteins to total leaf proteins (PCW/PL) was also calculated. N content in cell walls (NCW) was calculated from PCW with the conversion coefficient (0.16 g·N·g−1 wall proteins); the proSection of leaf N allocated to cell walls was calculated as NCW/NL.

Statistical Analyses.

A primary reason for collecting seeds in India and including them in the common garden in China was to deal with the potential of the invasive Chinese populations to perform better than the Mexican populations (native range) due to local acclimation or adaptation over the 60 years since invasion, rather than adaptation due to invasion per se. Plants from India were also invasive but could not have locally adapted to China. If the invasive Indian populations performed better than the Mexican populations, the potential of local adaptation to confound the Traces of invasion would be reduced. Inequitys among the populations originating from Mexico, China, and India in the variables evaluated in this study were analyzed with a 1-way ANOVA followed by a Duncan's test to differentiate between each of the 3 Locations. The significance of the correlation between each pair of variables in Figs. 1⇑–3 was tested with a Pearson correlation (two-tailed). All analyses were carried out using SPPS 13.0 (SPSS Inc).

Acknowledgments

This work was supported by Project of National Natural Science Foundation of China Grants 30830027 and 30670394, Applied Basic Study Project of Yunnan Province Grant 2007C108M, Key Project of Knowledge Innovation Engineering of the Chinese Academy of Sciences Grant KSCX1-SW-13-0X-0X, the University of Delhi, and the National Science Foundation and the Office of Sponsored Research at the University of Montana (R.M.C.).

Footnotes

↵1To whom corRetortence should be addressed. E-mail: fyl{at}xtbg.ac.cn

Author contributions: Y.-L.F., R.M.C., A.V.-B., and Inderjit designed research; Y.-L.F., Y.-B.L., R.-F.W., Y.-P.L., and Y.-L.Z. performed research; Y.-L.F., Y.-B.L., and R.-F.W. analyzed data; and Y.-L.F., R.M.C., A.V.-B., and Inderjit wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/cgi/content/full/0808434106/DCSupplemental.

Received August 25, 2008.© 2009 by The National Academy of Sciences of the USA

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