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The Robert H. Smith Institute of
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in Agriculture
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Publications

2020
Glanz-Idan, N. ; Wolf, S. Upregulation of photosynthesis in mineral nutrition-deficient tomato plants by reduced source-to-sink ratio. Plant Signaling & BehaviorPlant Signaling & Behavior 2020, 15, 1712543. Publisher's VersionAbstract
ABSTRACTPhotosynthetic activity is affected by environmental factors and endogenous signals controlled by the source?sink relationship. We recently showed upregulated photosynthetic rate following partial defoliation under favorable environmental conditions. Here, we examined the influence of partial defoliation on the remaining leaves? function in tomato plants under nutrient deficiency. The effect of partial defoliation was more pronounced under limited mineral supply vs. favorable conditions. Reduced source?sink ratio resulted in increased stomatal conductance and transpiration rate, as well as higher photosystem II efficiency. Although chlorophyll concentration was significantly reduced under limited nutrient supply, the photosynthetic rate in the remaining leaf was similar to that measured under normal fertilization. Expression of genes involved in the phloem loading of assimilated sugars was downregulated in the remaining source leaf of unfertilized plants, 15 d after partial defoliation; in fertilized plants, these genes? expression was similar in control and partially defoliated plants. We propose that at early stage, the additional carbon assimilated in the remaining leaf is devoted to increasing source size rather than sink growth. The size increase of the remaining leaf in unfertilized plants was not sufficient to rebalance the source?sink ratio, resulting in inhibited sugar export and further carbohydrate allocation in the remaining leaf.
Glanz-Idan, N. ; Wolf, S. Upregulation of photosynthesis in mineral nutrition-deficient tomato plants by reduced source-to-sink ratio. Plant Signal Behav 2020, 15, 1712543.Abstract
Photosynthetic activity is affected by environmental factors and endogenous signals controlled by the source-sink relationship. We recently showed upregulated photosynthetic rate following partial defoliation under favorable environmental conditions. Here, we examined the influence of partial defoliation on the remaining leaves' function in tomato plants under nutrient deficiency. The effect of partial defoliation was more pronounced under limited mineral supply vs. favorable conditions. Reduced source-sink ratio resulted in increased stomatal conductance and transpiration rate, as well as higher photosystem II efficiency. Although chlorophyll concentration was significantly reduced under limited nutrient supply, the photosynthetic rate in the remaining leaf was similar to that measured under normal fertilization. Expression of genes involved in the phloem loading of assimilated sugars was downregulated in the remaining source leaf of unfertilized plants, 15 d after partial defoliation; in fertilized plants, these genes' expression was similar in control and partially defoliated plants. We propose that at early stage, the additional carbon assimilated in the remaining leaf is devoted to increasing source size rather than sink growth. The size increase of the remaining leaf in unfertilized plants was not sufficient to rebalance the source-sink ratio, resulting in inhibited sugar export and further carbohydrate allocation in the remaining leaf.
Glanz-Idan, N. ; Tarkowski, P. ; Turečková, V. ; Wolf, S. Root-shoot communication in tomato plants: cytokinin as a signal molecule modulating leaf photosynthetic activity. Journal of experimental botany 2020, 71, 247-257. Publisher's VersionAbstract
Photosynthetic activity is affected by exogenous and endogenous inputs, including source-sink balance. Reducing the source to sink ratio by partial defoliation or heavy shading resulted in significant elevation of the photosynthetic rate in the remaining leaf of tomato plants within 3 d. The remaining leaf turned deep green, and its area increased by almost 3-fold within 7 d. Analyses of photosynthetic activity established up-regulation due to increased carbon fixation activity in the remaining leaf, rather than due to altered water balance. Moreover, senescence of the remaining leaf was significantly inhibited. As expected, carbohydrate concentration was lower in the remaining leaf than in the control leaves; however, expression of genes involved in sucrose export was significantly lower. These results suggest that the accumulated fixed carbohydrates were primarily devoted to increasing the size of the remaining leaf. Detailed analyses of the cytokinin content indicated that partial defoliation alters cytokinin biosynthesis in the roots, resulting in a higher concentration of trans-zeatin riboside, the major xylem-translocated molecule, and a higher concentration of total cytokinin in the remaining leaf. Together, our findings suggest that trans-zeatin riboside acts as a signal molecule that traffics from the root to the remaining leaf to alter gene expression and elevate photosynthetic activity. © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology.
2017
Shilo, T. ; Rubin, B. ; Plakhine, D. ; Gal, S. ; Amir, R. ; Hacham, Y. ; Wolf, S. ; Eizenberg, H. Secondary Effects of Glyphosate Action in Phelipanche aegyptiaca: Inhibition of Solute Transport from the Host Plant to the Parasite. Frontiers in Plant Science 2017, 8 255. Publisher's VersionAbstract
It is currently held that glyphosate efficiently controls the obligate holoparasite Phelipanche aegyptiaca (Egyptian broomrape) by inhibiting its endogenous shikimate pathway, thereby causing a deficiency in aromatic amino acids (AAA). While there is no argument regarding the shikimate pathway being the primary site of the herbicide's action, the fact that the parasite receives a constant supply of nutrients, including proteins and amino acids, from the host does not fit with an AAA deficiency. This apparent contradiction implies that glyphosate mechanism of action in P. aegyptiaca is probably more complex and does not end with the inhibition of the AAA biosynthetic pathway alone. A possible explanation would lie in a limitation of the translocation of solutes from the host as a secondary effect. We examined the following hypotheses: (a) glyphosate does not affects P. aegyptiaca during its independent phase and (b) glyphosate has a secondary effect on the ability of P. aegyptiaca to attract nutrients, limiting the translocation to the parasite. By using a glyphosate-resistant host plant expressing the “phloem-mobile” green fluorescent protein (GFP), it was shown that glyphosate interacts specifically with P. aegyptiaca, initiating a deceleration of GFP translocation to the parasite within 24 h of treatment. Additionally, changes in the entire sugars profile (together with that of other metabolites) of P. aegyptiaca were induced by glyphosate. In addition, glyphosate did not impair germination or seedling development of P. aegyptiaca but begun to exert its action only after the parasite has established a connection to the host vascular system and became exposed to the herbicide. Our findings thus indicate that glyphosate does indeed have a secondary effect in P. aegyptiaca, probably as a consequence of its primary target inhibition—via inhibition of the translocation of phloem-mobile solutes to the parasite, as was simulated by the mobile GFP. The observed disruption in the metabolism of major sugars that are abundant in P. aegyptiaca within 48 h after glyphosate treatment provides a possible explanation for this inhibition of translocation and might reflect a critical secondary effect of the herbicide's primary action that results in loss of the parasite's superior sink for solutes.
Spiegelman, Z. ; Shahar, A. ; Wolf, S. Down-regulation of SlCyp1 in the phloem reduces auxin response and photosynthetic rate in tomato (Solanum lycopersicum) plants. Plant Signal Behav 2017, 12, e1338224.Abstract
The tomato dgt mutant, containing a single mutation in the Cyclophilin1 (SlCyp1) gene, is auxin insensitive and exhibits a pleotropic phenotype that includes lack of lateral roots, malformed xylem structure and reduced root-to-shoot ratio. Recently, we found that the SlCyp1 protein is phloem-mobile and traffic from shoot to root to induce lateral root formation. These processes are achieved through activation of auxin-mediated developmental programs. Inhibition of the trafficked SlCyp1 activity at the target site resulted in inhibition of the auxin response, supporting the hypothesis that this protein is indeed a mobile signal. Here, we show that partial silencing of SlCyp1 in the phloem only resulted in perturbed auxin response in the roots and reduced photosynthetic and transpiration rates. The presented data suggests that expression of SlCyp1 in the phloem is essential for proper auxin response at the whole plant level. We, therefore, propose that this protein acts as a long-distance signaling molecule acting as coordinator between roots and shoot activities.
Spiegelman, Z. ; Omer, S. ; Mansfeld, B. N. ; Wolf, S. Function of Cyclophilin1 as a long-distance signal molecule in the phloem of tomato plants. J Exp Bot 2017, 68, 953-964.Abstract
Tomato (Solanum lycopersicum) diageotropica (dgt) mutants, containing a single mutation in the Cyclophilin1 (SlCyp1) gene, are auxin-insensitive, exhibiting a pleiotropic phenotype including lack of geotropism, abnormal xylem structure, lack of lateral roots (LRs), and elevated shoot-to-root ratio. SlCyp1 is a putative peptidyl-prolyl isomerase that can traffic from shoot to root, where it induces changes in auxin response, LR formation, and xylem development, suggesting it has a role as a long-distance signaling molecule. Here, we explored the mechanism underlying SlCyp1 function in the phloem. Expression of SlCyp1 under a phloem-specific (AtSuc2) promoter in dgt plants partially restored the wild-type phenotype, including lateral root development, root branching, and xylem morphology. The observed developmental changes were associated with physiological alternations at the whole-plant level, including a reduction in shoot-to-root ratio, enhanced transpiration, and elevated photosynthetic rates. Conversely, phloem-specific expression of SlCyp1 active-site mutants did not restore the wild-type phenotype. Local inhibition of cyclophilin functioning in the target tissue reduced auxin sensitivity, suggesting that its enzymatic activity in the distant organ is required for its action as a long-distance signalling agent. The data presented suggest that SlCyp1 is a signal molecule trafficking from shoot to root where its activity is required for auxin-mediated lateral root development.
2016
Shilo, T. ; Zygier, L. ; Rubin, B. ; Wolf, S. ; Eizenberg, H. Mechanism of glyphosate control of Phelipanche aegyptiaca. 2016, 244, 1095 - 1107. Publisher's VersionAbstract
Despite its total reliance on its host plant, the holoparasitePhelipanche aegyptiacasuffers from a deficiency of aromatic amino acids upon exposure to glyphosate.
2015
Spiegelman, Z. ; Ham, B. - K. ; Zhang, Z. ; Toal, T. W. ; Brady, S. M. ; Zheng, Y. ; Fei, Z. ; Lucas, W. J. ; Wolf, S. A tomato phloem-mobile protein regulates the shoot-to-root ratio by mediating the auxin response in distant organs. Plant J 2015, 83, 853-63.Abstract
The plant vascular system serves as a conduit for delivery of both nutrients and signaling molecules to various distantly located organs. The anucleate sieve tube system of the angiosperm phloem delivers sugars and amino acids to developing organs, and has recently been shown to contain a unique population of RNA and proteins. Grafting studies have established that a number of these macromolecules are capable of moving long distances between tissues, thus providing support for operation of a phloem-mediated inter-organ communication network. Currently, our knowledge of the roles played by such phloem-borne macromolecules is in its infancy. Here, we show that, in tomato, translocation of a phloem-mobile cyclophilin, SlCyp1, from a wild-type scion into a mutant rootstock results in restoration of vascular development and lateral root initiation. This process occurs through reactivation of auxin response pathways and reprogramming of the root transcriptome. Moreover, we show that long-distance trafficking of SlCyp1 is associated with regulation of the shoot-to-root ratio in response to changing light intensities, by modulating root growth. We conclude that long-distance trafficking of SlCyp1 acts as a rheostat to control the shoot-to-root ratio, by mediating root development to integrate photosynthesis and light intensity with requirements for access to water and mineral nutrients.