Damage-induced root nitrogen metabolism inNicotiana sylvestris: Testing C/N predictions for alkaloid production

Baldwin, Ian Thomas; Oesch, Robert C.; Merhige, Patricia M.; Hayes, Karen

doi:10.1007/bf00980600

Cited by 33 publications

(20 citation statements)

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“…In many plants the reduction of NO À 3 to NH 4 can occur in both root or shoot tissues, but NO À 3 is more eciently reduced in leaves (reviewed in Oaks and Hirel 1985;Oaks 1992) due to the availability of carbon and reductant from photosynthesis. In N. sylvestris, only 4% of a plant's nitrate reductase (NR) activity is in the roots (Baldwin et al 1993), which corresponds to the proportion of NO À 3 uptake that is used for nicotine biosynthesis in uninduced plants (Baldwin et al 1994c). However, neither root nor shoot NR is wound-inducible (Baldwin et al 1993), and since de novo nicotine synthesis increases after wounding to incorporate 7±9% of current N uptake (Baldwin et al 1994c), the additional reduced N required likely comes from the shoot reduction of NO À 3 in NO À 3 grown plants.…”

Section: Discussionmentioning

confidence: 99%

“…In N. sylvestris, only 4% of a plant's nitrate reductase (NR) activity is in the roots (Baldwin et al 1993), which corresponds to the proportion of NO À 3 uptake that is used for nicotine biosynthesis in uninduced plants (Baldwin et al 1994c). However, neither root nor shoot NR is wound-inducible (Baldwin et al 1993), and since de novo nicotine synthesis increases after wounding to incorporate 7±9% of current N uptake (Baldwin et al 1994c), the additional reduced N required likely comes from the shoot reduction of NO À 3 in NO À 3 grown plants. Hence, if plants grew in environments with a reliable supply of NH 4 , the induced nicotine response could function independently of shoot NR activity and allow plants to launch a complete induced response even when the entire canopy has been removed by herbivores.…”

Section: Discussionmentioning

confidence: 99%

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Fire, nitrogen, and defensive plasticity in Nicotiana attenuata

Lynds

Baldwin

1998

Oecologia

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Nicotiana attenuata is a post-fire annual that utilizes jasmonate-inducible nicotine production as an inducible chemical defense which, in turn, can utilize 6% of a plant' s nitrogen budget and be costly to seed production. We characterize the nitrogen pools of burned soils in the plant' s native environment (piñyon-juniper woodlands) and examine how variation in nitrogen source and supply rate influence the patterns of allocation to growth and inducible and constitutive nicotine production. Available soil nitrogen increases dramatically (40-fold) immediately after a fire and consists principally of ammonia which is subsequently oxidized to nitrate during post-fire succession. We simulate these changes in nitrogen availability in hydroponic culture and use allometric techniques to characterize changes in allocation. In two experiments, we alter (1) nitrate supply rates 8-fold and (2) the ratio of ammonia:nitrate under consistent nitrogen supply rates. In both experiments, we increase the allocation to nicotine by treating roots with methyl jasmonate (MJ), the methyl ester of the plant' s internal wound signal, jasmonic acid, which increases nicotine production in the roots after shoot herbivory. MJ treatments decrease whole plant (WP) growth, increase root:shoot ratio, and increase WP nicotine pools in all nitrogen environments. Overall, source and supply rate of nitrogen have no effect on either the constitutive or induced allometric relationships of nicotine accumulation and growth. This remarkable homeostasis in allocation patterns contradicts a key prediction of carbon nutrient (C/N) theory. With N-pulse-chase techniques, we demonstrate that plants preferentially utilize ammonia for nicotine production over nitrate when both nitrogen sources are available. This preferential use of ammonia may allow N. attenuata to reduce the biochemical costs of producing nicotine in the post-fire environment.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Fire, nitrogen, and defensive plasticity in Nicotiana attenuata

Lynds

Baldwin

1998

Oecologia

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“…We have established (Baldwin 1989, Baldwin et al 1993) that leaf damage results in dramatic increases in the concentration of nicotine in the xylem fluid, and therefore an examination of nicotine in xylem fluid is likely to reflect the pool of nicotine most recently synthesized in the roots. We have established (Baldwin 1989, Baldwin et al 1993) that leaf damage results in dramatic increases in the concentration of nicotine in the xylem fluid, and therefore an examination of nicotine in xylem fluid is likely to reflect the pool of nicotine most recently synthesized in the roots.…”

Section: Plant Growth Parameters and Experimental Conditionsmentioning

confidence: 99%

“…We have documented that leaf damage increases the concentration of nicotine in the xylem fluid exported from the roots of damaged plants without increasing the rate of nitrate reduction in the roots, and this increase in nicotine concentration occurs with a concurrent decrease in the concentration of amino acids and amides exported in the xylem fluid from the roots (Baldwin et al 1993). Here we use 15 N0 3 to first determine how quickly nitrogen can be absorbed, reduced, assimilated, and incorporated in nicotine.…”

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confidence: 99%

Allocation of 15N from Nitrate to Nicotine: Production and Turnover of a Damage‐Induced Mobile Defense

Baldwin¹,

Karb²,

Ohnmeiss³

1994

Ecology

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Nicotine is thought to be an excellent example of a "mobile" (sensu Coley et al. 1985) plant defense metabolite: it is synthesized in the roots, transported to leaves, and reported to be metabolically labile, with a half-life of <24 h. In a companion paper (Ohnmeiss and Baldwin 1994), we demonstrated that nondestructive damage dramatically increased the whole-plant allometric accumulation of nicotine in Nicotiana sylvestris (Solanaceae) and that damaged plants accumulated a larger proportion of their total nitrogen in nicotine pools than did undamaged plants. These damage-induced accumulations could arise from either increased nicotine production and/or decreased turnover with unaltered production. Here we ask how much of the change in whole-plant nicotine pools that is induced by damage is a result of increased nicotine production, with nitrogen derived from 15 N0 3 that was acquired, reduced, and assimilated after damage. In three experiments, we examine the rates of induced and constitutive nicotine production over 2 d, over 8 d under two nitrate supply rates, and over the lifetime of the plant. By examining 15 N-labeled nicotine pool sizes at different times after damage, we estimate the magnitudes of nicotine turnover and its importance in the induced changes in whole-plant nicotine pools.Two days after damage, damaged plants had accumulated 4.8 times the nicotine pool of undamaged plants, and 57% of the increase in the nicotine pool of damaged plants was synthesized with N from 15 N0 3 acquired after damage. Damage increased the rate of nicotine-N 15 production from 2.0 J.tg/h in undamaged plants to 6.3 J.tg/h in damaged plants.No evidence for nicotine turnover was found in either damaged or undamaged plants. The 8-d experiment conducted under two different nitrate supply rates confirmed these results. Furthermore, the 8-d experiment documented that N from 15 N0 3 acquired after damage was allocated to nicotine production in constant proportions within damaged and undamaged plants, independently of nitrate supply rate; 3.0-3.1 and 5. 7-6.1% of the total 15 N pool in undamaged and damaged plants, respectively, was used for nicotine production. Therefore, leaf damage doubles the allocation of recently acquired nitrogen to nicotine production in plants that do not differ in nitrate uptake or growth. In an experiment lasting 41 d after damage, we found that the damage-induced increase in total nicotine pools quantified after 5 d remained unchanged over the lifetime of the plants and that in undamaged plants the nicotine-' 5 N pool produced after 5 d was similarly unchanged at 41 d. In damaged plants the nicotine-15 N pool produced after 5 d decreased by 33.3% after 41 d. This decrease in the nicotine-15 N pools of damaged plants could be due to either metabolism or volatilization.We conclude that nicotine is not the metabolically labile secondary metabolite that it has been previously reported to be and that the changes in pool sizes induced by damage and nitrogen stress are principally due to changes in prod...

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“…Diverse experiments quantifying biosynthesis and transport demonstrate that nicotine is synthesized largely in the roots and transported to the shoot in the xylem stream. (Dawson 1942;Baldwin 1989Baldwin , 1991Baldwin et al 1993Baldwin et al , 1994b. Moreover, the key regulatory enzyme in nicotine biosynthesis, putrescine N-methyltransferase and the mRNA coding for this enzyme, is wound-inducible and localized in the roots (Mizusaki et al 1973;Saunders and Bush 1979;Feth et al 1986;Hibi et al 1994).…”

Section: Introductionmentioning

confidence: 97%

Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris

Baldwin

Zhang

Diab

et al. 1997

Planta

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283

201

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Jasmonic acid (JA) is thought to be part of a signal-transduction pathway which dramatically increases de-novo nicotine synthesis in the roots and increases whole-plant (WP) nicotine pools in response to the wounding of the leaves in Nicotiana sylvestrisSpegazzini and Comes (Solanaceae). We report the synthesis of a doubly labeled JA ([1, 2-13 C]JA) and use it as an internal standard to quantify by gas chromatography-mass spectrometry the changes in root and shoot JA pools in plants subjected to differing amounts of standardized leaf wounding. Wounding increased JA pools 10-fold locally in damaged leaves within 90 min and systemically in the roots (3.5-fold) 180 min after wounding. If JA functions as an intermediary between stimulus and response, quantitative relationships among the stimulus, JA, and the response should exist. To examine these relationships, we varied the number of punctures in four leaves and quantified both the resulting JA in damaged leaves after 90 min and the resulting WP nicotine concentration after 5 d. We found statistically significant, positive relationships among number of leaf punctures, endogenous JA, and WP nicotine accumulation. We used two inhibitors of wound-induced nicotine production, methyl salicylate and indole-3-acetic acid, to manipulate the relationships between wound-induced changes in JA and WP nicotine accumulation. Since wounding and the response to wounding occur in widely separated tissues, we applied inhibitors to different plant parts to examine their effects on the local and systemic components of this response. In all experiments, inhibition of the wound-induced increase in leaf JA 90 min after wounding was associated with the inhibition of the nicotine response 5 d after wounding. We conclude that wound-induced increases in leaf JA are an important component of this longdistance signal-transduction pathway.Abbreviations: JA = jasmonic acid; WP = whole plant; MSA = methyl salicylate

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Damage-induced root nitrogen metabolism inNicotiana sylvestris: Testing C/N predictions for alkaloid production

Cited by 33 publications

References 25 publications

Fire, nitrogen, and defensive plasticity in Nicotiana attenuata

Fire, nitrogen, and defensive plasticity in Nicotiana attenuata

Allocation of 15N from Nitrate to Nicotine: Production and Turnover of a Damage‐Induced Mobile Defense

Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris

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