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A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast- and slow-growing Populus hybrid clones.

Harding SA, Jarvie MM, Lindroth RL, Tsai CJ - J. Exp. Bot. (2009)

Bottom Line: Carbon partitioning within phenylpropanoid and carbohydrate networks in developing stems differed sharply between clones.The results did not support the idea that foliar production of phenylpropanoid defence chemicals was the primary cause of reduced plant growth in the slow-growing clone.The findings are discussed in the context of metabolic mechanism(s) which may contribute to reduced N delivery from roots to leaves, thereby compromising tree growth and promoting leaf phenolic accrual in the slow-growing clone.

View Article: PubMed Central - PubMed

Affiliation: School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA. sharding@uga.edu

ABSTRACT
The biosynthetic costs of phenylpropanoid-derived condensed tannins (CTs) and phenolic glycosides (PGs) are substantial. However, despite reports of negative correlations between leaf phenolic content and growth of Populus, it remains unclear whether or how foliar biosynthesis of CT/PG interferes with tree growth. A comparison was made of carbon partitioning and N content in developmentally staged leaves, stems, and roots of two closely related Populus hybrid genotypes. The genotypes were selected as two of the most phytochemically divergent from a series of seven previously analysed clones that exhibit a range of height growth rates and foliar amino acid, CT, and PG concentrations. The objective was to analyse the relationship between leaf phenolic content and plant growth, using whole-plant carbon partitioning and N distribution data from the two divergent clones. Total N as a percentage of tissue dry mass was comparatively low, and CT and PG accrual comparatively high in leaves of the slow-growing clone. Phenylpropanoid accrual and N content were comparatively high in stems of the slow-growing clone. Carbon partitioning within phenylpropanoid and carbohydrate networks in developing stems differed sharply between clones. The results did not support the idea that foliar production of phenylpropanoid defence chemicals was the primary cause of reduced plant growth in the slow-growing clone. The findings are discussed in the context of metabolic mechanism(s) which may contribute to reduced N delivery from roots to leaves, thereby compromising tree growth and promoting leaf phenolic accrual in the slow-growing clone.

Show MeSH
Proposed phenylpropanoid effects on N distribution and vascular development in SG and FG. Enhanced lignification in roots and lower stems of SG is proposed to reduce N distribution, represented by the term ‘flux’, into upper internodes. A decrease in foliar %N results, which favours starch and CT accrual at the expense of cellulose deposition in developing vascular traces. With less cellulose scaffolding, lignification is reduced and NSPs such as the PGs become the predominant phenylpropanoids. Ultimately, both reduced vascular development and high sugar demand for NSP biosynthesis interfere with the provision to expanding leaves in SG.
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fig8: Proposed phenylpropanoid effects on N distribution and vascular development in SG and FG. Enhanced lignification in roots and lower stems of SG is proposed to reduce N distribution, represented by the term ‘flux’, into upper internodes. A decrease in foliar %N results, which favours starch and CT accrual at the expense of cellulose deposition in developing vascular traces. With less cellulose scaffolding, lignification is reduced and NSPs such as the PGs become the predominant phenylpropanoids. Ultimately, both reduced vascular development and high sugar demand for NSP biosynthesis interfere with the provision to expanding leaves in SG.

Mentions: A unifying and interpretive scenario of the present findings is shown in Fig. 8. A cumulative effect of some metabolic process(s) in roots and stems on N distribution is posited to reduce the provision of N to expanding leaves while promoting pooling of N in SG stems. While starch and CT were both elevated in leaves of SG, consistent with a perceived N limitation, cellulose accrual was lower than in FG. In contrast to FG, there was not a correlation between foliar starch and cellulose contents in SG. The absence of a correlation could reflect strong interference by competing synthetic activities for starch-derived glucose in SG. Under the circumstances of lower foliar N in SG, CT synthesis could be an important alternative destination for starch glucose. Because cellulose precedes lignin deposition during secondary cell wall growth (Mellerowicz et al., 2001), reduced cellulose synthesis could have interfered with lignification of vascular traces, explaining the reduced xylem fluorescence in elongating internodes of SG (Figs 4, 5). A loop would thereby be constituted in which reduced vascular growth in upper stems further impeded N delivery to leaves. In general, the scenario illustrates how the relatively low amino acid concentrations commonly observed in leaf metabolic profiles of slower growing, high foliar NSP clones (Harding et al., 2005) could reflect a foliar N limitation, due to an inefficient transport system and/or an N-sequestering process in secondary stems and roots.


A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast- and slow-growing Populus hybrid clones.

Harding SA, Jarvie MM, Lindroth RL, Tsai CJ - J. Exp. Bot. (2009)

Proposed phenylpropanoid effects on N distribution and vascular development in SG and FG. Enhanced lignification in roots and lower stems of SG is proposed to reduce N distribution, represented by the term ‘flux’, into upper internodes. A decrease in foliar %N results, which favours starch and CT accrual at the expense of cellulose deposition in developing vascular traces. With less cellulose scaffolding, lignification is reduced and NSPs such as the PGs become the predominant phenylpropanoids. Ultimately, both reduced vascular development and high sugar demand for NSP biosynthesis interfere with the provision to expanding leaves in SG.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2724693&req=5

fig8: Proposed phenylpropanoid effects on N distribution and vascular development in SG and FG. Enhanced lignification in roots and lower stems of SG is proposed to reduce N distribution, represented by the term ‘flux’, into upper internodes. A decrease in foliar %N results, which favours starch and CT accrual at the expense of cellulose deposition in developing vascular traces. With less cellulose scaffolding, lignification is reduced and NSPs such as the PGs become the predominant phenylpropanoids. Ultimately, both reduced vascular development and high sugar demand for NSP biosynthesis interfere with the provision to expanding leaves in SG.
Mentions: A unifying and interpretive scenario of the present findings is shown in Fig. 8. A cumulative effect of some metabolic process(s) in roots and stems on N distribution is posited to reduce the provision of N to expanding leaves while promoting pooling of N in SG stems. While starch and CT were both elevated in leaves of SG, consistent with a perceived N limitation, cellulose accrual was lower than in FG. In contrast to FG, there was not a correlation between foliar starch and cellulose contents in SG. The absence of a correlation could reflect strong interference by competing synthetic activities for starch-derived glucose in SG. Under the circumstances of lower foliar N in SG, CT synthesis could be an important alternative destination for starch glucose. Because cellulose precedes lignin deposition during secondary cell wall growth (Mellerowicz et al., 2001), reduced cellulose synthesis could have interfered with lignification of vascular traces, explaining the reduced xylem fluorescence in elongating internodes of SG (Figs 4, 5). A loop would thereby be constituted in which reduced vascular growth in upper stems further impeded N delivery to leaves. In general, the scenario illustrates how the relatively low amino acid concentrations commonly observed in leaf metabolic profiles of slower growing, high foliar NSP clones (Harding et al., 2005) could reflect a foliar N limitation, due to an inefficient transport system and/or an N-sequestering process in secondary stems and roots.

Bottom Line: Carbon partitioning within phenylpropanoid and carbohydrate networks in developing stems differed sharply between clones.The results did not support the idea that foliar production of phenylpropanoid defence chemicals was the primary cause of reduced plant growth in the slow-growing clone.The findings are discussed in the context of metabolic mechanism(s) which may contribute to reduced N delivery from roots to leaves, thereby compromising tree growth and promoting leaf phenolic accrual in the slow-growing clone.

View Article: PubMed Central - PubMed

Affiliation: School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA. sharding@uga.edu

ABSTRACT
The biosynthetic costs of phenylpropanoid-derived condensed tannins (CTs) and phenolic glycosides (PGs) are substantial. However, despite reports of negative correlations between leaf phenolic content and growth of Populus, it remains unclear whether or how foliar biosynthesis of CT/PG interferes with tree growth. A comparison was made of carbon partitioning and N content in developmentally staged leaves, stems, and roots of two closely related Populus hybrid genotypes. The genotypes were selected as two of the most phytochemically divergent from a series of seven previously analysed clones that exhibit a range of height growth rates and foliar amino acid, CT, and PG concentrations. The objective was to analyse the relationship between leaf phenolic content and plant growth, using whole-plant carbon partitioning and N distribution data from the two divergent clones. Total N as a percentage of tissue dry mass was comparatively low, and CT and PG accrual comparatively high in leaves of the slow-growing clone. Phenylpropanoid accrual and N content were comparatively high in stems of the slow-growing clone. Carbon partitioning within phenylpropanoid and carbohydrate networks in developing stems differed sharply between clones. The results did not support the idea that foliar production of phenylpropanoid defence chemicals was the primary cause of reduced plant growth in the slow-growing clone. The findings are discussed in the context of metabolic mechanism(s) which may contribute to reduced N delivery from roots to leaves, thereby compromising tree growth and promoting leaf phenolic accrual in the slow-growing clone.

Show MeSH