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1.  How does timing, duration and severity of heat stress influence pollen-pistil interactions in angiosperms? 
Plant Signaling & Behavior  2011;6(7):930-933.
Reproductive development in sexual plants is substantially more sensitive to high temperature stress than vegetative development, resulting in negative implications for food and fiber production under the moderate temperature increases projected to result from global climate change. High temperature exposure either during early pollen development or during the progamic phase of pollen development will negatively impact pollen performance and reproductive output; both phases of pollen development are considered exceptionally sensitive to moderate heat stress. However, moderately elevated temperatures either before or during the progamic phase can limit fertilization by negatively impacting important pollen pistil interactions required for successful pollen tube growth toward the ovules. This mini-review identifies the impacts of heat stress on pollen-pistil interactions and sexual reproduction in angiosperms. A special emphasis is placed on the biochemical response of the pistil to moderately high temperature and the resultant influence on in vivo pollen performance and fertilization.
PMCID: PMC3257764  PMID: 21628998
pollen-pistil interaction; carbohydrates; heat stress; fertilization; pollen tube growth; climate change
2.  Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response 
Journal of Experimental Botany  2009;60(13):3891-3908.
Above-optimal temperatures reduce yield in tomato largely because of the high heat stress (HS) sensitivity of the developing pollen grains. The high temperature response, especially at this most HS-sensitive stage of the plant, is poorly understood. To obtain an overview of molecular mechanisms underlying the HS response (HSR) of microspores, a detailed transcriptomic analysis of heat-stressed maturing tomato microspores was carried out using a combination of Affymetrix Tomato Genome Array and cDNA-amplified fragment length polymorphism (AFLP) techniques. The results were corroborated by reverse transcription-PCR (RT-PCR) and immunoblot analyses. The data obtained reveal the involvement of specific members of the small heat shock protein (HSP) gene family, HSP70 and HSP90, in addition to the HS transcription factors A2 (HSFA2) and HSFA3, as well as factors other than the classical HS-responsive genes. The results also indicate HS regulation of reactive oxygen species (ROS) scavengers, sugars, plant hormones, and regulatory genes that were previously implicated in other types of stress. The use of cDNA-AFLP enabled the detection of genes representing pollen-specific functions that are missing from the tomato Affymetrix chip, such as those involved in vesicle-mediated transport and a pollen-specific, calcium-dependent protein kinase (CDPK2). For several genes, including LeHSFA2, LeHSP17.4-CII, as well as homologues of LeHSP90 and AtVAMP725, higher basal expression levels were detected in microspores of cv. Hazera 3042 (a heat-tolerant cultivar) compared with microspores of cv. Hazera 3017 (a heat-sensitive cultivar), marking these genes as candidates for taking part in microspore thermotolerance. This work provides a comprehensive analysis of the molecular events underlying the HSR of maturing microspores of a crop plant, tomato.
PMCID: PMC2736902  PMID: 19628571
cDNA-AFLP; gene expression; heat stress response; microarray; microspore maturation; tomato
3.  Further analysis of XBAT32, an Arabidopsis RING E3 ligase, involved in ethylene biosynthesis 
Plant Signaling & Behavior  2010;5(11):1425-1429.
The Arabidopsis RING E3 ligase, XBAT32, was previously characterized as a regulator of lateral root initiation. However, how XBAT32 function to modulate lateral root initiation was unknown. In our recent paper, we demonstrated that XBAT32 is involved in ethylene biosynthesis and it is through this function that XBAT32 is able to regulate lateral root production. Here we discuss a few other findings, observed in the ethylene overproducing mutant, xbat32, that reflect the effect of elevated ethylene levels on plant growth and development. Ethylene signaling also regulates plant responses to adverse environmental conditions such as high salinity. Consistent with ethylene's role as a stress hormone, xbat32 exhibited increased sensitivity to salt stress during seed germination and postgerminative growth. Thus, XBAT32 may also play a role in ethylene mediated response to abiotic stresses.
PMCID: PMC3115245  PMID: 21051934
Arabidopsis thaliana; ethylene; lateral root; RING E3 ligase; salt stress; ubiquitination
4.  ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation 
Journal of Clinical Investigation  2005;115(8):2169-2179.
Pollen exposure induces allergic airway inflammation in sensitized subjects. The role of antigenic pollen proteins in the induction of allergic airway inflammation is well characterized, but the contribution of other constituents in pollen grains to this process is unknown. Here we show that pollen grains and their extracts contain intrinsic NADPH oxidases. The pollen NADPH oxidases rapidly increased the levels of ROS in lung epithelium as well as the amount of oxidized glutathione (GSSG) and 4-hydroxynonenal (4-HNE) in airway-lining fluid. These oxidases, as well as products of oxidative stress (such as GSSG and 4-HNE) generated by these enzymes, induced neutrophil recruitment to the airways independent of the adaptive immune response. Removal of pollen NADPH oxidase activity from the challenge material reduced antigen-induced allergic airway inflammation, the number of mucin-containing cells in airway epithelium, and antigen-specific IgE levels in sensitized mice. Furthermore, challenge with Amb a 1, the major antigen in ragweed pollen extract that does not possess NADPH oxidase activity, induced low-grade allergic airway inflammation. Addition of GSSG or 4-HNE to Amb a 1 challenge material boosted allergic airway inflammation. We propose that oxidative stress generated by pollen NADPH oxidases (signal 1) augments allergic airway inflammation induced by pollen antigen (signal 2).
PMCID: PMC1180538  PMID: 16075057
5.  Cross-talk between sulfur assimilation and ethylene signaling in plants 
Plant Signaling & Behavior  2012;8(1):e22478.
Sulfur (S) deficiency is prevailing all over the world and becoming an important issue for crop improvement through maximising its utilization efficiency by plants for sustainable agriculture. Its interaction with other regulatory molecules in plants is necessary to improve our understanding on its role under changing environment. Our knowledge on the influence of S on ethylene signaling is meagre although it is a constituent of cysteine (Cys) required for the synthesis of reduced glutathione (GSH) and S-adenosyl methionine (SAM), a precursor of ethylene biosynthesis. Thus, there may be an interaction between S assimilation, ethylene signaling and plant responses under optimal and stressful environmental conditions. The present review emphasizes that responses of plants to S involve ethylene action. This evaluation will provide an insight into the details of interactive role of S and ethylene signaling in regulating plant processes and prove profitable for developing sustainability under changing environmental conditions.
PMCID: PMC3745555  PMID: 23104111
abiotic stress; cysteine; ethylene biosynthesis; ethylene signaling; glutathione; sulfur assimilation
6.  Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers 
Journal of Experimental Botany  2009;61(2):453-462.
The high sensitivity of male reproductive cells to high temperatures may be due to an inadequate heat stress response. The results of a comprehensive expression analysis of HsfA2 and Hsp17-CII, two important members of the heat stress system, in the developing anthers of a heat-tolerant tomato genotype are reported here. A transcriptional analysis at different developmental anther/pollen stages was performed using semi-quantitative and real-time PCR. The messengers were localized using in situ RNA hybridization, and protein accumulation was monitored using immunoblot analysis. Based on the analysis of the gene and protein expression profiles, HsfA2 and Hsp17-CII are finely regulated during anther development and are further induced under both short and prolonged heat stress conditions. These data suggest that HsfA2 may be directly involved in the activation of protection mechanisms in the tomato anther during heat stress and, thereby, may contribute to tomato fruit set under adverse temperatures.
PMCID: PMC2803211  PMID: 19854799
Anther development; heat stress; HsfA2; Hsp17-CII; pollen; tomato
7.  Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis 
Journal of Experimental Botany  2010;61(14):3901-3914.
Mature pollen is very sensitive to cold stress in chilling-sensitive plants. Plant WRKY DNA-binding transcription factors are key regulators in plant responses to abiotic and biotic stresses. Previous studies have suggested that WRKY34 (At4g26440) gene might be involved in pollen viability, although the mechanism involved is unclear. In this study, it is shown that cold treatment increased WRKY34 expression in the wild type, and promoter-GUS analysis revealed that WRKY34 expression is pollen-specific. Enhanced green fluorescent protein-tagged WRKY34 was localized in the nuclei. Pollen harbouring the wrky34 allele showed higher viability than pollen with the WRKY34 allele after cold treatment. Further functional analysis indicated that the WRKY34 transcription factor was involved in pollen development regulated by the pollen-specific MIKC* class of MADS-domain transcription factors under cold stress, and cold-insensitivity of mature wrky34 pollen might be partly attributable to the enhanced expression of transcriptional activator CBFs in the mutants. Thus, the WRKY34 transcription factor negatively mediated cold sensitivity of mature Arabidopsis pollen and might be involved in the CBF signal cascade in mature pollen.
PMCID: PMC2935866  PMID: 20643804
Arabidopsis; cold stress; pollen; transcription factor; WRKY34
8.  Ectopic Overexpression of SlHsfA3, a Heat Stress Transcription Factor from Tomato, Confers Increased Thermotolerance and Salt Hypersensitivity in Germination in Transgenic Arabidopsis 
PLoS ONE  2013;8(1):e54880.
Plant heat stress transcription factors (Hsfs) are the critical components involved in mediating responses to various environmental stressors. However, the detailed roles of many plant Hsfs are far from fully understood. In this study, an Hsf (SlHsfA3) was isolated from the cultivated tomato (Solanum lycopersicum, Sl) and functionally characterized at the genetic and developmental levels. The nucleus-localized SlHsfA3 was basally and ubiquitously expressed in different plant organs. The expression of SlHsfA3 was induced dramatically by heat stress, moderately by high salinity, and slightly by drought, but was not induced by abscisic acid (ABA). The ectopic overexpression of SlHsfA3 conferred increased thermotolerance and late flowering phenotype to transgenic Arabidopsis plants. Moreover, SlHsfA3 played a negative role in controlling seed germination under salt stress. RNA-sequencing data demonstrated that a number of heat shock proteins (Hsps) and stress-associated genes were induced in Arabidopsis plants overexpressing SlHsfA3. A gel shift experiment and transient expression assays in Nicotiana benthamiana leaves demonstrated that SlHsfA3 directly activates the expression of SlHsp26.1-P and SlHsp21.5-ER. Taken together, our results suggest that SlHsfA3 behaves as a typical Hsf to contribute to plant thermotolerance. The late flowering and seed germination phenotypes and the RNA-seq data derived from SlHsfA3 overexpression lines lend more credence to the hypothesis that plant Hsfs participate in diverse physiological and biochemical processes related to adverse conditions.
PMCID: PMC3551807  PMID: 23349984
9.  Pollen-Induced Oxidative Stress Influences Both Innate and Adaptive Immune Responses via Altering Dendritic Cell Functions 
It has been demonstrated that pollen grains contain NAD(P)H oxidases that induce oxidative stress in the airways, and this oxidative insult is critical for the development of allergic inflammation in sensitized mice. On the basis of this observation, we have examined whether pollen grain exposure triggers oxidative stress in dendritic cells (DCs), altering their functions. To test this hypothesis, human monocyte-derived DCs were treated with ragweed pollen grains. Our findings show that exposure to pollen grains induces an increase in the intracellular levels of reactive oxygen species in DCs. Our data also indicate that besides the NAD(P)H oxidases, other component(s) of pollen grains contributes to this phenomenon. Elevated levels of intracellular reactive oxygen species triggered the production of IL-8 as well as proinflammatory cytokines, such as TNF-α and IL-6. Treatment with pollen grains initiated the maturation of DCs, strongly upregulated the membrane expression of CD80, CD86, CD83, and HLA-DR, and caused only a slight increase in the expression of CD40. The pollen-treated DCs induced the development of naive T lymphocytes toward effector T cells with a mixed profile of cytokine production. Antioxidant inhibited both the phenotypic and functional changes of DCs, underlining the importance of oxidative stress in these processes. Collectively, these data show that pollen exposure-induced oxidative stress may contribute to local innate immunity and participate in the initiation of adaptive immune responses to pollen Ags.
PMCID: PMC3028537  PMID: 20118277
10.  Induction of alternative respiratory pathway involves nitric oxide, hydrogen peroxide and ethylene under salt stress 
Plant Signaling & Behavior  2010;5(12):1636-1637.
Alternative respiratory pathway (AP) plays an important role in plant thermogenesis, fruit ripening and responses to environmental stresses. AP may participate in the adaptation to salt stress since salt stress increased the activity of the AP. Recently, new evidence revealed that ethylene and hydrogen peroxide (H2O2) are involved in the salt-induced increase of the AP, which plays an important role in salt tolerance in Arabidopsis callus, and ethylene may be acting downstream of H2O2. Recent observations also indicated both ethylene and nitric oxide (NO) act as signaling molecules in responses to salt stress, and ethylene may be a part of the downstream signal molecular in NO action. In this addendum, a hypothetical model for NO function in regulation of H2O2- and ethylene-mediated induction of AP under salt stress is presented.
PMCID: PMC3115120  PMID: 21139431
alternative respiratory pathway; ethylene; hydrogen peroxide; nitric oxide; salt stress; signaling molecule
11.  Immunological Interactive Effects between Pollen Grains and Their Cytoplasmic Granules on Brown Norway Rats 
Grass pollen is one of the most important aeroallergen vectors in Europe. Under some meteorological factors, pollen grains can release pollen cytoplasmic granules (PCGs). PCGs induce allergic responses. Several studies have shown that during a period of thunderstorms the number of patients with asthma increases because of higher airborne concentrations of PCGs.
The aims of the study were to assess the allergenicity of interactive effects between pollen and PCGs and to compare it with allergenicity of Timothy grass pollen and PCGs in Brown Norway rats.
Rats were sensitized (day 0) and challenged (day 21) with pollen grains and/or PCGs. Four groups were studied: pollen-pollen (PP), PCGs-PCGs (GG), pollen-PCGs (PG), and PCGs-pollen (GP). Blood samples, bronchoalveolar lavage fluid, and bronchial lymph node were collected at day 25. IgE and IgG1 levels in sera were assessed by enzyme-linked immunosorbent assay. Alveolar cells, protein, and cytokine concentrations were quantified in bronchoalveolar lavage fluid. T-cell proliferation, in response to pollen or granules, was performed by lymph node assay.
Interactive effects between pollen and PCGs increased IgE and IgG1 levels when compared with those of the negative control. These increases were lower than those of the PP group but similar to the levels obtained by the GG group. Whatever was used in the sensitization and/or challenge phase, PCGs increased lymphocyte and Rantes levels compared with those of the pollen group. The interactive effects increased IL-1α and IL-1β compared with those of the PP and GG groups.
Immunologic interactive effects have been shown between pollen and PCGs. For humoral and cellular allergic responses, interactive effects between the 2 aeroallergenic sources used in this study seem to be influenced mainly by PCGs.
PMCID: PMC3650983  PMID: 23283149
immunologic interactive effects; timothy grass pollen; pollen cytoplasmic granules; allergy; inflammation
12.  The Plant Growth Promoting Substance, Lumichrome, Mimics Starch, and Ethylene-Associated Symbiotic Responses in Lotus and Tomato Roots 
Symbiosis involves responses that maintain the plant host and symbiotic partner’s genetic program; yet these cues are far from elucidated. Here we describe the effects of lumichrome, a flavin identified from Rhizobium spp., applied to lotus (Lotus japonicus) and tomato (Solanum lycopersicum). Combined transcriptional and metabolite analyses suggest that both species shared common pathways that were altered in response to this application under replete, sterile conditions. These included genes involved in symbiosis, as well as transcriptional and metabolic responses related to enhanced starch accumulation and altered ethylene metabolism. Lumichrome priming also resulted in altered colonization with either Mesorhizobium loti (for lotus) or Glomus intraradices/G. mossea (for tomato). It enhanced nodule number but not nodule formation in lotus; while leading to enhanced hyphae initiation and delayed arbuscule maturation in tomato.
PMCID: PMC3371600  PMID: 22701462
ethylene; flavin; lumichrome; mycorrhiza; nodulation; starch; symbiosis
13.  The coordinated role of ethylene and glucose in sulfur-mediated protection of photosynthetic inhibition by cadmium 
Plant Signaling & Behavior  2012;7(11):1420-1422.
Ethylene controls photosynthesis and induces tolerance of plants to metal stress. However, little is known about the interaction between ethylene, photosynthesis and sulfur (S) availability under cadmium (Cd) stress. Recently, we reported that ethylene controls photosynthesis by increasing glutathione (GSH) synthesis with sufficient-S availability under Cd stress. Plants treated with Cd were less sensitive to ethylene and showed photosynthetic inhibition. Ethylene sensitivity of plants was increased with exogenously-sourced ethylene or with sufficient-S application resulting in induced GSH synthesis and alleviation of photosynthetic inhibition by Cd. In this addendum we present some additional data indicating that ethylene regulates photosynthesis by reducing glucose (Glc) sensitivity, thus reducing the Glc-mediated photosynthetic repression.
PMCID: PMC3548862  PMID: 22951406
ethylene; glucose sensitivity; glutathione; sugars; photosynthesis
14.  Sublethal concentrations of salicylic acid decrease the formation of reactive oxygen species but maintain an increased nitric oxide production in the root apex of the ethylene-insensitive Never ripe tomato mutants 
Plant Signaling & Behavior  2011;6(9):1263-1266.
The pattern of salicylic acid (SA)-induced production of reactive oxygen species (ROS) and nitric oxide (NO) were different in the apex of adventitious roots in wild-type and in the ethylene-insensitive Never ripe (Nr) mutants of tomato (Solanum lycopersicum L. cv Ailsa Craig). ROS were upregulated, while NO remained at the control level in apical root tissues of wildtype plants exposed to sublethal concentrations of SA. In contrast, Nr plants expressing a defective ethylene receptor displayed a reduced level of ROS and a higher NO content in the apical root cells. In wild-type plants NO production seems to be ROS(H2O2)-dependent at cell death-inducing concentrations of SA, indicating that ROS and NO may interact to trigger oxidative cell death. In the absence of significant ROS accumulation, the increased NO production caused moderate reduction in cell viability in root apex of Nr plants exposed to 10−3 M SA. This suggests that a functional ethylene signaling pathway is necessary for the control of ROS and NO production induced by SA.
PMCID: PMC3258047  PMID: 21847015
ethylene receptor mutant; never ripe; nitric oxide; reactive oxygen species; root apex; salicylic acid; tomato
15.  Availability of Micro-Tom mutant library combined with TILLING in molecular breeding of tomato fruit shelf-life 
Breeding Science  2012;62(2):202-208.
Novel mutant alleles of an ethylene receptor Solanum lycopersicum ETHYLENE RESPONSE1 (SlETR1) gene, Sletr1-1 and Sletr1-2, were isolated from the Micro-Tom mutant library by TILLING in our previous study. They displayed different levels of impaired fruit ripening phenotype, suggesting that these alleles could be a valuable breeding material for improving shelf life of tomato fruit. To conduct practical use of the Sletr1 alleles in tomato breeding, genetic complementation analysis by transformation of genes carrying each allele is required. In this study, we generated and characterized transgenic lines over-expressing Sletr1-1 and Sletr1-2. All transgenic lines displayed ethylene insensitive phenotype and ripening inhibition, indicating that Sletr1-1 and Sletr1-2 associate with the ethylene insensitive phenotype. The level of ethylene sensitivity in the seedling was different between Sletr1-1 and Sletr1-2 transgenic lines, whereas no apparent difference was observed in fruit ripening phenotype. These results suggested that it is difficult to fine-tune the extent of ripening by transgenic approach even if the weaker allele (Sletr1-2) was used. Our present and previous studies indicate that the Micro-Tom mutant library combined with TILLING could be an efficient tool for exploring genetic variations of important agronomic traits in tomato breeding.
PMCID: PMC3405968  PMID: 23136532
ethylene receptor; tomato fruit shelf-life; Micro-Tom; molecular breeding; TILLING; transgenic tomato
16.  Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene 
BMC Plant Biology  2012;12:190.
The phytohormone ethylene is involved in a wide range of developmental processes and in mediating plant responses to biotic and abiotic stresses. Ethylene signalling acts via a linear transduction pathway leading to the activation of Ethylene Response Factor genes (ERF) which represent one of the largest gene families of plant transcription factors. How an apparently simple signalling pathway can account for the complex and widely diverse plant responses to ethylene remains yet an unanswered question. Building on the recent release of the complete tomato genome sequence, the present study aims at gaining better insight on distinctive features among ERF proteins.
A set of 28 cDNA clones encoding ERFs in the tomato (Solanum lycopersicon) were isolated and shown to fall into nine distinct subclasses characterised by specific conserved motifs most of which with unknown function. In addition of being able to regulate the transcriptional activity of GCC-box containing promoters, tomato ERFs are also shown to be active on promoters lacking this canonical ethylene-responsive-element. Moreover, the data reveal that ERF affinity to the GCC-box depends on the nucleotide environment surrounding this cis-acting element. Site-directed mutagenesis revealed that the nature of the flanking nucleotides can either enhance or reduce the binding affinity, thus conferring the binding specificity of various ERFs to target promoters.
Based on their expression pattern, ERF genes can be clustered in two main clades given their preferential expression in reproductive or vegetative tissues. The regulation of several tomato ERF genes by both ethylene and auxin, suggests their potential contribution to the convergence mechanism between the signalling pathways of the two hormones.
The data reveal that regions flanking the core GCC-box sequence are part of the discrimination mechanism by which ERFs selectively bind to their target promoters. ERF tissue-specific expression combined to their responsiveness to both ethylene and auxin bring some insight on the complexity and fine regulation mechanisms involving these transcriptional mediators. All together the data support the hypothesis that ERFs are the main component enabling ethylene to regulate a wide range of physiological processes in a highly specific and coordinated manner.
PMCID: PMC3548740  PMID: 23057995
Ethylene; ERF; Transcriptional regulation; cis-regulatory elements; Tomato
17.  Transport of airborne Picea schrenkiana pollen on the northern slope of Tianshan Mountains (Xinjiang, China) and its implication for paleoenvironmental reconstruction 
Aerobiologia  2012;29(2):161-173.
The understanding of airborne pollen transportation is crucial for the reconstruction of the paleoenvironment. Under favorable conditions, a considerable amount of long-distance-transported pollen can be deposited far from its place of origin. In extreme arid regions, in most cases, such situations occur and increase the difficulty to interpret fossil pollen records. In this study, three sets of Cour airborne pollen trap were installed on the northern slope of Tianshan Mountains to collect airborne Picea schrenkiana (spruce) pollen grains from July 2001 to July 2006. The results indicate that Picea pollen disperses extensively and transports widely in the lower atmosphere far away from spruce forest. The airborne Picea pollen dispersal period is mainly concentrated between mid-May and July. In desert area, weekly Picea pollen began to increase and peaked suddenly in concentration. Also, annual pollen indices do not decline even when the distance increased was probably related to the strong wind may pick up the deposited pollen grains from the topsoil into the air stream, leading to an increase of pollen concentration in the air that is irrelevant to the normal and natural course of pollen transport and deposition. This, in turn, may lead to erroneous interpretations of the pollen data in the arid region. This study provided insight into the shift in the Picea pollen season regarding climate change in arid areas. It is recorded that the pollen pollination period starts earlier and the duration became longer. The results also showed that the temperature of May and June was positively correlated with the Picea pollen production. Furthermore, the transport of airborne Picea pollen data is useful for interpreting fossil pollen records from extreme arid regions.
PMCID: PMC3618411  PMID: 23576840
Cour method; Pollen dispersion; Sandstorm; Aerobiology; Climate change; Vegetation history; Arid regions
18.  Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants 
Journal of Experimental Botany  2008;59(15):4119-4131.
Following exposure to salinity, the root/shoot ratio is increased (an important adaptive response) due to the rapid inhibition of shoot growth (which limits plant productivity) while root growth is maintained. Both processes may be regulated by changes in plant hormone concentrations. Tomato plants (Solanum lycopersicum L. cv Moneymaker) were cultivated hydroponically for 3 weeks under high salinity (100 mM NaCl) and five major plant hormones (abscisic acid, ABA; the cytokinins zeatin, Z, and zeatin-riboside, ZR; the auxin indole-3-acetic acid, IAA; and the ethylene precursor 1-aminocyclopropane-1-carboxylic acid, ACC) were determined weekly in roots, xylem sap, and leaves. Salinity reduced shoot biomass by 50–60% and photosynthetic area by 20–25% both by decreasing leaf expansion and delaying leaf appearance, while root growth was less affected, thus increasing the root/shoot ratio. ABA and ACC concentrations strongly increased in roots, xylem sap, and leaves after 1 d (ABA) and 15 d (ACC) of salinization. By contrast, cytokinins and IAA were differentially affected in roots and shoots. Salinity dramatically decreased the Z+ZR content of the plant, and induced the conversion of ZR into Z, especially in the roots, which accounted for the relative increase of cytokinins in the roots compared to the leaf. IAA concentration was also strongly decreased in the leaves while it accumulated in the roots. Decreased cytokinin content and its transport from the root to the shoot were probably induced by the basipetal transport of auxin from the shoot to the root. The auxin/cytokinin ratio in the leaves and roots may explain both the salinity-induced decrease in shoot vigour (leaf growth and leaf number) and the shift in biomass allocation to the roots, in agreement with changes in the activity of the sink-related enzyme cell wall invertase.
PMCID: PMC2639025  PMID: 19036841
Abscisic acid; 1-aminocyclopropane-1-carboxylic acid; indole-3-acetic acid; plant hormones; salt stress; sodium chloride; tomato (Solanum lycopersicum L.); zeatin; zeatin-riboside
19.  Fused lobed anther and hooked stigma affect pollination, fertilization and fruit set in mango 
Plant Signaling & Behavior  2013;8(3):e23167.
Mango malformation is the most threaten disease that limits mango production, worldwide. For a long time, due to its complex nature, the cause and causal agents were strongly disputed. Diverse Fusaria, including Fusarium mangiferae, are known to be associated with the disease. There are indications that augmented level of endogenous ethylene in response to various abiotic and biotic stresses alters the morphology of reproductive organs. Here, scanning electron microscopy (SEM) of healthy and malformed reproductive organs of mango cv. Baramasi was performed to compare the functional morphology. The SEM study revealed that anthers of hermaphrodite healthy flowers were bilobed with large number of turgid pollen grains whereas malformed flowers showed fused lobed anthers with scanty deformed pollen grains. Furthermore, the stigma of healthy flowers exhibited a broad landing pad as compared to malformed stigma which showed hooked and pointed tip. All these impaired morphology of male and female reproductive organs lead to failure of sexual reproduction. This is the first evidence to show fused lobed anther with impaired pollen grains and hooked stigma with poor stigmatic receptivity are mainly responsible for restricting the pollen germination and pollen tube growth. Here we suggest that abnormal development of anthers and pistils is due to endogenously produced stress ethylene. Further, added load of cyanide, a byproduct of ethylene biosynthesis, may also contribute to the development of necrosis which lead to desiccation of anther and pistil during hypersensitive response of plants.
PMCID: PMC3676485  PMID: 23299320
Anther; mango malformation; pollen; scanning electron microscopy; stigma; stress ethylene
20.  Pollen density on the stigma affects endogenous gibberellin metabolism, seed and fruit set, and fruit quality in Pyrus pyrifolia 
Journal of Experimental Botany  2010;61(15):4291-4302.
To clarify the relationship between pollen density and gametophytic competition in Pyrus pyrifolia, gametophytic performance, gibberellin metabolism, fruit set, and fruit quality were investigated by modifying P. pyrifolia pollen grain number and density with Lycopodium spores. Higher levels of pollen density improved seed viability, fruit set, and fruit quality. Treatments with the highest pollen density showed a significantly increased fruit growth rate and larger fruit at harvest. High pollen density increased germination rate and gave a faster pollen tube growth, both in vivo and in vitro. Endogenous gibberellin (GA) concentrations increased in pollen tubes soon after germination and the concentration of two growth-active GAs, GA3, and GA4, was positively correlated to final fruit size, cell numbers in the mesocarp, and pollen tube growth rate. These two GAs appear to be biosynthesized de novo in pollen tube and are the main pollen-derived bioactive GAs found after pollen germination. GA1 levels in the pollen tube appear to be related to a pollen–style interaction that occurred after the pollen grains landed on the stigma.
PMCID: PMC2955744  PMID: 20713466
Gametophytic competition; gibberellins; pollen density; pollination; Pyrus pyrifolia
21.  Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard 
Journal of Experimental Botany  2011;62(14):4955-4963.
In order to ascertain the stomatal and photosynthetic responses of mustard to ethylene under varying N availability, photosynthetic characteristics of mustard grown with optimal (80 mg N kg−1 soil) or low (40 mg N kg−1 soil) N were studied after the application of an ethylene-releasing compound, ethephon (2-chloroethyl phosphonic acid) at 40 days after sowing (DAS). The availability of N influenced ethylene evolution and affected stomatal conductance and photosynthesis. The effect of ethylene was smaller under deficient N where plants contained higher glucose (Glc) sensitivity, despite high ethylene evolution even in the absence of ethephon, potentially because the plants were less sensitive to ethylene per se. Ethephon application at each level of N increased ethylene and decreased Glc sensitivity, which increased photosynthesis via its effect on the photosynthetic machinery and effects on stomatal conductance. Plants grown with sufficient-N and treated with 200 μl l−1 ethephon exhibited optimal ethylene, the greatest stomatal conductance and photosynthesis, and growth. These plants made maximum use of available N and exhibited the highest nitrogen-use efficiency (NUE).
PMCID: PMC3193011  PMID: 21705383
Ethephon; ethylene; glucose; nitrogen-use efficiency; photosynthesis
22.  Convergence of developmental mutants into a single tomato model system: 'Micro-Tom' as an effective toolkit for plant development research 
Plant Methods  2011;7:18.
The tomato (Solanum lycopersicum L.) plant is both an economically important food crop and an ideal dicot model to investigate various physiological phenomena not possible in Arabidopsis thaliana. Due to the great diversity of tomato cultivars used by the research community, it is often difficult to reliably compare phenotypes. The lack of tomato developmental mutants in a single genetic background prevents the stacking of mutations to facilitate analysis of double and multiple mutants, often required for elucidating developmental pathways.
We took advantage of the small size and rapid life cycle of the tomato cultivar Micro-Tom (MT) to create near-isogenic lines (NILs) by introgressing a suite of hormonal and photomorphogenetic mutations (altered sensitivity or endogenous levels of auxin, ethylene, abscisic acid, gibberellin, brassinosteroid, and light response) into this genetic background. To demonstrate the usefulness of this collection, we compared developmental traits between the produced NILs. All expected mutant phenotypes were expressed in the NILs. We also created NILs harboring the wild type alleles for dwarf, self-pruning and uniform fruit, which are mutations characteristic of MT. This amplified both the applications of the mutant collection presented here and of MT as a genetic model system.
The community resource presented here is a useful toolkit for plant research, particularly for future studies in plant development, which will require the simultaneous observation of the effect of various hormones, signaling pathways and crosstalk.
PMCID: PMC3146949  PMID: 21714900
hormonal mutants; Solanum lycopersicum; model organism; photomorphogenesis; plant development
23.  Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions 
Journal of Experimental Botany  2013;65(1):261-273.
Ethylene-mediated reactive oxygen species signalling is involved in adaptive responses of wheat seedlings to waterlogged conditions through controlling formation of lysigenous aerenchyma and expression of genes encoding ethanol fermentation enzymes in roots
Exposing plants to hypoxic conditions greatly improves their anoxic stress tolerance by enhancing the activities of glycolysis and fermentation in roots. Ethylene may also be involved in these adaptive responses because its synthesis is increased in roots under hypoxic conditions. Here it is reported that pre-treatment of wheat seedlings with an ethylene precursor, 1-aminocyclopropanecarboxylic acid (ACC), enhanced accumulation of ethylene in the roots of wheat seedlings, and enhanced their tolerance of oxygen-deficient conditions through increasing the expression of genes encoding ethanol fermentation enzymes, alcohol dehydrogenase and pyruvate decarboxylase, in the roots. Lysigenous aerenchyma formation in root was induced by ACC pre-treatment and was further induced by growth under oxygen-deficient conditions. ACC pre-treatment increased the expression of three genes encoding respiratory burst oxidase homologue (a plant homologue of gp91phox in NADPH oxidase), which has a role in the generation of reactive oxygen species (ROS), in roots of seedlings. Co-treatment with ACC and an NADPH oxidase inhibitor, diphenyleneiodonium, partly suppressed the ACC-induced responses. These results suggest that ethylene and ROS are involved in adaptation of wheat seedlings to oxygen-deficient conditions through controlling lysigenous aerenchyma formation and the expression of genes encoding ethanol fermentation enzymes.
PMCID: PMC3883296  PMID: 24253196
Aerenchyma; ethylene; fermentation; oxygen deficiency; reactive oxygen species; wheat (Triticum aestivum L.).
24.  19 Proteomic Analysis of Major and Minor Allergens From Isolated Pollen Cytoplasmic Granules 
Grass pollen is one of the most important vectors of aeroallergens. Under atmospheric conditions, pollen grains can release pollen cytoplasmic granules (PCGs). The allergens associated with these intrinsic sub-fractions induce, in laboratory animals as well as in asthmatic patients allergic and inflammatory responses. The aims of this study were to characterize and identify the intrinsic allergens of PCGs, to compare them with those of pollen grains.
PCGs were isolated from Phleum pratense pollen by osmotic shock. The water-soluble proteins were extracted from pollen grains and their PCGs. Nine out of 26 grass sensitized patient sera were selected on the basis of previous ELISA and immunoblotting results showing IgE specific binding to numerous grass pollen allergens. IgE-binding proteins were analyzed by 1- and 2D-immunobloting using grass pollen-sensitized patient sera. Once located, allergens were characterized by mass spectrometry.
2D gels of pollen and PCGs extract revealed about 100 and 40 proteins respectively, with a large spectrum of Mr (10–>94 kDa) and pI (<4.5–10.0). More proteins as well as more allergens in pollen than in PCGs were detected by immunoblotting. Several of the allergens listed in the IUIS nomenclature - Phl p 1, 4, 5, 6, 11 and 12 - were found in pollen and PCGs extracts while Phl p 11 was found only in PCGs and Phl p 2 as well as Phl p 13 only in pollen extract. Some other allergens, not listed in the IUIS nomenclature, were also characterized in both pollen and PCGs extracts.
Since the major grass pollen allergens were found in PCGs and because of their small size, these sub-micronic particles should be considered as very potent sensitizing and challenging respirable vectors of allergens. We demonstrate here that PCGs are at least as much dangerous as pollen grains.
PMCID: PMC3513069
25.  Ethylene independent induction of lycopene biosynthesis in tomato fruits by jasmonates 
Journal of Experimental Botany  2012;63(16):5751-5761.
One of the main characteristics of tomato (Solanum lycopersicum) fruit ripening is a massive accumulation of carotenoids (mainly lycopene), which may contribute to the nutrient quality of tomato fruit and its role in chemoprevention. Previous studies have shown that ethylene (ET) plays a central role in promoting fruit ripening. In this study, the role of jasmonic acid (JA) in controlling lycopene accumulation in tomato fruits was analysed by measuring fruit lycopene content and the expression levels of lycopene biosynthetic genes in JA-deficient mutants (spr2 and def1) and a 35S::prosystemin transgenic line (35S::prosys) with increased JA levels and constitutive JA signalling. The lycopene content was significantly decreased in the fruits of spr2 and def1, but was enhanced in 35S::prosys fruits. Simultaneously, the expression of lycopene biosynthetic genes followed a similar trend. Lycopene synthesis in methyl jasmonate (MeJA) vapour-treated fruits showed an inverted U-shaped dose response, which significantly enhanced the fruit lycopene content and restored lycopene accumulation in spr2 and def1 at a concentration of 0.5 µM. The results indicated that JA plays a positive role in lycopene biosynthesis. In addition, the role of ET in JA-induced lycopene accumulation was also examined. Ethylene production in tomato fruits was depressed in spr2 and def1 while it increased in 35S::prosys. However, the exogenous application of MeJA to Never ripe (Nr), the ET-insensitive mutant, significantly promoted lycopene accumulation, as well as the expression of lycopene biosynthetic genes. Based on these results, it is proposed that JA might function independently of ethylene to promote lycopene biosynthesis in tomato fruits.
PMCID: PMC3467294  PMID: 22945939
Ethylene (ET); fruit; jasmonic acid (JA); lycopene; mutant; tomato

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