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The importance of aboveground-belowground interactions on the evolution and maintenance of variation in plant defense traits.

van Geem M, Gols R, van Dam NM, van der Putten WH, Fortuna T, Harvey JA - Front Plant Sci (2013)

Bottom Line: Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts.For instance, although our understanding of genetic variation in aboveground plant traits and its effects on community-level interactions is well developed, little is known about the importance of aboveground-belowground interactions in driving this variation.In nature, these trade-offs may critically depend upon their effects on plant fitness.

View Article: PubMed Central - PubMed

Affiliation: Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW) Wageningen, Netherlands.

ABSTRACT
Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts. Aboveground-belowground studies have thus far focused on elucidating processes and underlying mechanisms that mediate the behavior and performance of invertebrates in opposite ecosystem compartments. Less is known about genetic variation in plant traits such as defense as that may be driven by above- and belowground trophic interactions. For instance, although our understanding of genetic variation in aboveground plant traits and its effects on community-level interactions is well developed, little is known about the importance of aboveground-belowground interactions in driving this variation. Plant traits may have evolved in response to selection pressures from above- and below-ground interactions from antagonists and mutualists. Here, we discuss gaps in our understanding of genetic variation in plant-related traits as they relate to aboveground and belowground multitrophic interactions. When metabolic resources are limiting, multiple attacks by antagonists in both domains may lead to trade-offs. In nature, these trade-offs may critically depend upon their effects on plant fitness. Natural enemies of herbivores may also influence selection for different traits via top-down control. At larger scales these interactions may generate evolutionary "hotspots" where the expression of various plant traits is the result of strong reciprocal selection via direct and indirect interactions. The role of abiotic factors in driving genetic variation in plant traits is also discussed.

No MeSH data available.


Related in: MedlinePlus

(A)Brassica oleracea. (B) Shoot and root glucosinolate levels (mean + SE of mean total, n = 4 or 5) of Brassica oleracea plants originating in Dorset, England from three wild populations located at sites called Kimmeridge (KIM), Old Harry (OH), and Winspit (WIN), respectively. Glucosinolates were classified according to their amino acid origin into indole, aromatic and aliphatic GS. The latter group was further divided into methylsulfinyl, alkenyl, and hydroxyl (=OH) GS. The plants were either untreated controls (CON), induced with 9 second instar Plutella xylostella (PLUT) larvae divided over three leaves, induced with 500 μg jasmonic acid either applied to the roots (RJA) or to the shoots (SJA). Jasmonic acid was used to simulate herbivory by chewing herbivores (Van Dam et al., 2004b). Roots and shoot tissues were harvested for GS analysis 7 days after the induction treatments. Different letter over the bars indicate significant differences (p < 0.05) in total glucosinolate level between the bars within each panel (Tukey HSD multiple comparisons among means). Please note the difference in scaling of the Y-axes. Both population and induction treatment had a significant effect on total GS levels in wild B. oleracea (MANOVA, treatment F6,82 = 5.77, p < 0.001; population F4,82 = 18.7, p < 0.001). All classes of GS, as well as total GS concentrations, differed with population origin in both the roots and the shoots (p < 0.05 for all analyses). In the shoots, indole GS (F3,42 = 23.9, p < 0.001) increased in response to the three induction treatments. Aromatic GS were also affected by induction treatment (F3,42 = 3.34, p = 0.03). Only WIN shoots contained small amounts of aromatic GS and these decreased with shoot induction, P. xylostella feeding and JA treatment, but increased with root JA application. In the roots, only indole GS responded significantly to induction treatment (F3,42 = 7.57, p < 0.001); JA applied to the roots increased indole GS levels in these tissues.
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Figure 2: (A)Brassica oleracea. (B) Shoot and root glucosinolate levels (mean + SE of mean total, n = 4 or 5) of Brassica oleracea plants originating in Dorset, England from three wild populations located at sites called Kimmeridge (KIM), Old Harry (OH), and Winspit (WIN), respectively. Glucosinolates were classified according to their amino acid origin into indole, aromatic and aliphatic GS. The latter group was further divided into methylsulfinyl, alkenyl, and hydroxyl (=OH) GS. The plants were either untreated controls (CON), induced with 9 second instar Plutella xylostella (PLUT) larvae divided over three leaves, induced with 500 μg jasmonic acid either applied to the roots (RJA) or to the shoots (SJA). Jasmonic acid was used to simulate herbivory by chewing herbivores (Van Dam et al., 2004b). Roots and shoot tissues were harvested for GS analysis 7 days after the induction treatments. Different letter over the bars indicate significant differences (p < 0.05) in total glucosinolate level between the bars within each panel (Tukey HSD multiple comparisons among means). Please note the difference in scaling of the Y-axes. Both population and induction treatment had a significant effect on total GS levels in wild B. oleracea (MANOVA, treatment F6,82 = 5.77, p < 0.001; population F4,82 = 18.7, p < 0.001). All classes of GS, as well as total GS concentrations, differed with population origin in both the roots and the shoots (p < 0.05 for all analyses). In the shoots, indole GS (F3,42 = 23.9, p < 0.001) increased in response to the three induction treatments. Aromatic GS were also affected by induction treatment (F3,42 = 3.34, p = 0.03). Only WIN shoots contained small amounts of aromatic GS and these decreased with shoot induction, P. xylostella feeding and JA treatment, but increased with root JA application. In the roots, only indole GS responded significantly to induction treatment (F3,42 = 7.57, p < 0.001); JA applied to the roots increased indole GS levels in these tissues.

Mentions: Various species of Brassicas differ in their GS profiles, both in AG and BG tissues (Figures 1 and 2). For example, the relative GS concentrations in AG and BG tissues differ dramatically, with root concentrations being much higher than shoot concentrations in Bunias orientalis, these being lower in B. nigra and similar in S. arvensis (Figure 1B). Usually, levels of GS are lower in BG than in AG tissues (Van Dam, 2009). Across species, variation in defense chemistry has been demonstrated to affect the performance of associated insects (Francis et al., 2001; Müller et al., 2002; Renwick, 2002; Harvey et al., 2003, 2010; Gols et al., 2008c). These dramatic differences in plant secondary chemistry at the species level may have implications for the interactions with other organisms in nature.


The importance of aboveground-belowground interactions on the evolution and maintenance of variation in plant defense traits.

van Geem M, Gols R, van Dam NM, van der Putten WH, Fortuna T, Harvey JA - Front Plant Sci (2013)

(A)Brassica oleracea. (B) Shoot and root glucosinolate levels (mean + SE of mean total, n = 4 or 5) of Brassica oleracea plants originating in Dorset, England from three wild populations located at sites called Kimmeridge (KIM), Old Harry (OH), and Winspit (WIN), respectively. Glucosinolates were classified according to their amino acid origin into indole, aromatic and aliphatic GS. The latter group was further divided into methylsulfinyl, alkenyl, and hydroxyl (=OH) GS. The plants were either untreated controls (CON), induced with 9 second instar Plutella xylostella (PLUT) larvae divided over three leaves, induced with 500 μg jasmonic acid either applied to the roots (RJA) or to the shoots (SJA). Jasmonic acid was used to simulate herbivory by chewing herbivores (Van Dam et al., 2004b). Roots and shoot tissues were harvested for GS analysis 7 days after the induction treatments. Different letter over the bars indicate significant differences (p < 0.05) in total glucosinolate level between the bars within each panel (Tukey HSD multiple comparisons among means). Please note the difference in scaling of the Y-axes. Both population and induction treatment had a significant effect on total GS levels in wild B. oleracea (MANOVA, treatment F6,82 = 5.77, p < 0.001; population F4,82 = 18.7, p < 0.001). All classes of GS, as well as total GS concentrations, differed with population origin in both the roots and the shoots (p < 0.05 for all analyses). In the shoots, indole GS (F3,42 = 23.9, p < 0.001) increased in response to the three induction treatments. Aromatic GS were also affected by induction treatment (F3,42 = 3.34, p = 0.03). Only WIN shoots contained small amounts of aromatic GS and these decreased with shoot induction, P. xylostella feeding and JA treatment, but increased with root JA application. In the roots, only indole GS responded significantly to induction treatment (F3,42 = 7.57, p < 0.001); JA applied to the roots increased indole GS levels in these tissues.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3842511&req=5

Figure 2: (A)Brassica oleracea. (B) Shoot and root glucosinolate levels (mean + SE of mean total, n = 4 or 5) of Brassica oleracea plants originating in Dorset, England from three wild populations located at sites called Kimmeridge (KIM), Old Harry (OH), and Winspit (WIN), respectively. Glucosinolates were classified according to their amino acid origin into indole, aromatic and aliphatic GS. The latter group was further divided into methylsulfinyl, alkenyl, and hydroxyl (=OH) GS. The plants were either untreated controls (CON), induced with 9 second instar Plutella xylostella (PLUT) larvae divided over three leaves, induced with 500 μg jasmonic acid either applied to the roots (RJA) or to the shoots (SJA). Jasmonic acid was used to simulate herbivory by chewing herbivores (Van Dam et al., 2004b). Roots and shoot tissues were harvested for GS analysis 7 days after the induction treatments. Different letter over the bars indicate significant differences (p < 0.05) in total glucosinolate level between the bars within each panel (Tukey HSD multiple comparisons among means). Please note the difference in scaling of the Y-axes. Both population and induction treatment had a significant effect on total GS levels in wild B. oleracea (MANOVA, treatment F6,82 = 5.77, p < 0.001; population F4,82 = 18.7, p < 0.001). All classes of GS, as well as total GS concentrations, differed with population origin in both the roots and the shoots (p < 0.05 for all analyses). In the shoots, indole GS (F3,42 = 23.9, p < 0.001) increased in response to the three induction treatments. Aromatic GS were also affected by induction treatment (F3,42 = 3.34, p = 0.03). Only WIN shoots contained small amounts of aromatic GS and these decreased with shoot induction, P. xylostella feeding and JA treatment, but increased with root JA application. In the roots, only indole GS responded significantly to induction treatment (F3,42 = 7.57, p < 0.001); JA applied to the roots increased indole GS levels in these tissues.
Mentions: Various species of Brassicas differ in their GS profiles, both in AG and BG tissues (Figures 1 and 2). For example, the relative GS concentrations in AG and BG tissues differ dramatically, with root concentrations being much higher than shoot concentrations in Bunias orientalis, these being lower in B. nigra and similar in S. arvensis (Figure 1B). Usually, levels of GS are lower in BG than in AG tissues (Van Dam, 2009). Across species, variation in defense chemistry has been demonstrated to affect the performance of associated insects (Francis et al., 2001; Müller et al., 2002; Renwick, 2002; Harvey et al., 2003, 2010; Gols et al., 2008c). These dramatic differences in plant secondary chemistry at the species level may have implications for the interactions with other organisms in nature.

Bottom Line: Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts.For instance, although our understanding of genetic variation in aboveground plant traits and its effects on community-level interactions is well developed, little is known about the importance of aboveground-belowground interactions in driving this variation.In nature, these trade-offs may critically depend upon their effects on plant fitness.

View Article: PubMed Central - PubMed

Affiliation: Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW) Wageningen, Netherlands.

ABSTRACT
Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts. Aboveground-belowground studies have thus far focused on elucidating processes and underlying mechanisms that mediate the behavior and performance of invertebrates in opposite ecosystem compartments. Less is known about genetic variation in plant traits such as defense as that may be driven by above- and belowground trophic interactions. For instance, although our understanding of genetic variation in aboveground plant traits and its effects on community-level interactions is well developed, little is known about the importance of aboveground-belowground interactions in driving this variation. Plant traits may have evolved in response to selection pressures from above- and below-ground interactions from antagonists and mutualists. Here, we discuss gaps in our understanding of genetic variation in plant-related traits as they relate to aboveground and belowground multitrophic interactions. When metabolic resources are limiting, multiple attacks by antagonists in both domains may lead to trade-offs. In nature, these trade-offs may critically depend upon their effects on plant fitness. Natural enemies of herbivores may also influence selection for different traits via top-down control. At larger scales these interactions may generate evolutionary "hotspots" where the expression of various plant traits is the result of strong reciprocal selection via direct and indirect interactions. The role of abiotic factors in driving genetic variation in plant traits is also discussed.

No MeSH data available.


Related in: MedlinePlus