Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink–source model of plant defense

Abstract

Summary• Here, we examine the influence of source-to-sink carbohydrate (CHO) flow on the development of constitutive and inducible levels of phenylpropenoids in hybrid poplar ( Populus nigra × P. deltoides ) foliage to determine if secondary metabolic processes in plant modules can be inhibited in a predictable manner by events such as herbivory and the development of new leaves and reproductive structures, which alter the path of phloem-borne resources.• Phenylpropenoid concentrations were determined for developing foliage after CHO flow, measured as the translocation of 13 C from labeled sources was manipulated.• Phenylpropenoid metabolism in both unwounded and induced sink leaves was directly and positively linked to rates of CHO import. Alterations in rates of translocation yielded different results, depending on how CHO import was affected: the removal of competing sinks rapidly and dramatically increased leaf phenolic contents, whereas phenolic levels (and their inducibility) tended to be reduced when import was interrupted.• High and inducible sink strength in developing poplar leaves provides resources for phenolic biosynthesis and, as a result, restrictions or re-directions of CHOs affect the foliar quality. Sink strength and the vascular architecture of plants, which confer upon them a modular nature, can determine the direction and magnitude of defense responses in trees.

Seagrass–pathogen interactions: ‘pseudo-induction’ of turtlegrass phenolics near wasting disease lesions

“…lesions damage vascular tissues in seagrass blades, disrupting the flow of carbohydrates within seagrass blades and resulting in accumulations of phenolics wherever carbohydrates are in overabundance, as predicted by Jones & Hartley (1999). Such responses are known from terrestrial plants, including birch, pine and poplar, and are predicted by the sink/source model of plant defense (Haukioja 1990, Tuomi et al 1991, Honkanen et al 1999, Arnold et al 2004). This model predicts that 'induced' responses arise when the allocation of carbon resources among tissues acting as carbohydrate sources and sinks is altered, e.g.…”

Alteration of plant primary metabolism in response to insect herbivory

“…For instance, herbivory on sorghum induced expression of nitrate and nitrite reductases that are required for nitrogen assimilation into Gln and Glu (Zhu-Salzman et al, 2004); expression of Glu synthase (also known as Gln oxoglutarate aminotransferase, or GOGAT) was induced by aphid feeding on N. attenuata (Voelckel et al, 2004); and aphid feeding induced Gln synthetase, which acts together with GOGAT in the Gln synthetase/GOGAT cycle, in celery (Apium graveolens; Divol et al, 2005). However, examination of multiple such data sets shows that either production or degradation amino acids can be preferred, depending on the specific plant-herbivore system being investigated and the type of tissue (local or systemic) being analyzed (Dorschner et al, 1987;Sandström et al, 2000;Arnold et al, 2004;Koyama et al, 2004;Caldana et al, 2011;Appel et al, 2012).…”

“…In methyl jasmonate-treated or wounded Arabidopsis, radioactively labeled carbohydrates were imported into sink leaves within hours after treatment, and were incorporated into defense-related compounds such as cinnamic acid and phenolic glycosides (Ferrieri et al, 2012). When carbohydrate import was disrupted by removing source leaves or cutting vascular connections, hybrid poplar (Populus deltoides 3 Populus nigra) defenses were induced less efficiently (Arnold and Schultz, 2002;Arnold et al, 2004). In contrast to carbohydrate transport, labeled nitrogen tracking studies have shown little evidence of jasmonic acid-induced nitrogen transport to elicited leaves in poplar (Arnold et al, 2004;Appel et al, 2012).…”

“…When carbohydrate import was disrupted by removing source leaves or cutting vascular connections, hybrid poplar (Populus deltoides 3 Populus nigra) defenses were induced less efficiently (Arnold and Schultz, 2002;Arnold et al, 2004). In contrast to carbohydrate transport, labeled nitrogen tracking studies have shown little evidence of jasmonic acid-induced nitrogen transport to elicited leaves in poplar (Arnold et al, 2004;Appel et al, 2012). Nevertheless, it is well established that defense-related nitrogenous compounds such as nicotine and other alkaloids are transported from roots to leaves upon insect attack (Baldwin et al, 1994;Hartmann and Ober, 2000;Ziegler and Facchini, 2008).…”

Carbohydrate, phenolic and antioxidant level in relation to chlorophyll a content in oilseed winter rape (Brassica napus L.) inoculated with Leptosphaeria maculans

“…Black squares -7 days after the inoculation; gray circles -14 days after the inoculation. The lines represent linear adjustment at a probability level P<0.05 (Arnold et al 2004) playing a key role in defense mechanisms during pathogenesis (Rusjan et al 2012;Hura et al 2014a, b). The results of some recent studies provided evidence that the high level of phenolic compounds can be linked with low susceptibility of plants to fungal infection (Mikulic-Petkovsek et al 2014a, b).…”