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Plant Physiology 148:671-672 (2008)
© 2008 American Society of Plant Biologists

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ON THE INSIDE

On the Inside


Carbon Monoxide: A Regulator of Plant Growth?

In animal cells, carbon monoxide (CO), mainly generated by heme oxygenases (HOs), is recognized as a significant modulator of inflammatory reactions. A search of the plant biological literature reveals scattered, largely forgotten reports of endogenous CO production by plants as well as CO effects on plant growth. For example, as long as 75 years ago, it was established that exogenous CO induces the initiation and stimulation of adventitious root in plants. In this issue, Xuan et al. (pp. 881–893) demonstrate that treatment of cucumber (Cucumis sativus) hypocotyls with the auxin transport inhibitor naphthylphthalamic acid (NPA) prevents auxin-mediated induction of adventitious rooting. The inhibition of adventitious rooting by NPA is associated with a decrease in HO activity and CO content. Moreover, the application of hematin, a HO activator and CO donor, or CO alone was able to alleviate indole acetic acid (IAA) depletion-induced inhibition of adventitious root formation. The addition of IAA or hematin rapidly increased HO protein expression and activity, as well as CO content. The effects of hematin were prevented by the simultaneous application of a HO-specific inhibitor. This HO-specific inhibitor mimicked the effects of NPA and caused the down-regulation of several IAA-induced proteins. Taken together, the data suggest that HO and CO act as novel downstream signal components in the auxin-induced pathway that leads to adventitious root formation in cucumber.


Nitrate Abundance Affects the Hydraulic Properties of Roots

Nitrogen availability in soils is often patchy. The roots of many plants respond to pockets of low nitrate availability in soils by locally enhancing extension growth and suppressing branching. Conversely, when encountering pockets rich in nitrate, a root will often proliferate locally to take advantage of this patch. Nitrate transporters and proteins involved in nitrate assimilation are also up-regulated in response to high exogenous nitrate concentrations. Thus, the plant devotes more biomass to a nitrate-rich patch, and the surface of this enhanced biomass is more efficient in absorbing nitrate. Although natural selection has given rise to these clever mechanisms, there is an additional problem that plants encounter: the local depletion of nitrate immediately near the root surface due either to increased uptake rates or to the fact that nitrate-rich patches can shift rapidly with mass flow of water in the soil. When there is a significant drop in nitrate concentration at the root surface, a coordinated increase in mass flow rates may be necessary to assure nitrate delivery and the maintenance of higher concentrations of nitrate near the root surface. Gorska et al. (pp. 1159–1167) report that variation in nitrate concentration around roots does indeed induce an immediate alteration of root hydraulic properties, such that water is preferentially absorbed from the nitrate-rich patch. Furthermore, they demonstrate that cellular nitrate levels, not the products of nitrate assimilation, are directly involved in changes of hydraulic membrane properties. By performing split-root experiments in which nitrate was applied to a portion of the root system, the authors demonstrate that the response is both localized and reversible, resulting in rapid changes in water uptake to the portions of the roots exposed to the nitrate-rich patch. At the same time, water uptake by roots not supplied with nitrate was reduced. The rapidity of this response allows plants to optimize resource acquisition in the face of environmental heterogeneity.


Plant Sperm Transcriptome

The two sperm cells produced by the pollen of angiosperms are transported by the elongating tube to the micropylar end of the embryo sac. There, they are released and double fertilization occurs. Understanding the mechanisms and conditions by which male gametes mature and take part in fertilization are crucial goals in the study of plant reproduction. Despite the fact that sperm cells have highly condensed chromatin, the original assumption that they are transcriptionally quiescent has been disproven by the identification of the AtGEX1 promoter, whose expression is confined to sperm cells. Transcriptome analyses of sperm cells in Arabidopsis (Arabidopsis thaliana) have previously not been possible because no method to isolate sperm cells was available. Borges et al. (pp. 1168–1181) have used a newly developed protocol, based on fluorescence-activated cell sorting, to isolate and purify sperm cells from transgenic Arabidopsis plants that were expressing enhanced GFP under the control of a sperm-specific promoter (AtGEX2::eGFP). This protocol allowed them to isolate enough pure sperm to allow Affymetrix ATH1 Genome Array analysis of the sperm cell transcriptome. The direct comparison of their transcriptome with those of pollen and seedlings, as well as with additional ATH1 data sets from a variety of vegetative tissues, showed that the sperm cell transcriptome was distinct and diverse. The functional classification of sperm-enriched transcripts showed that DNA repair, ubiquitin-mediated proteolysis, and proteins required for progression through the cell cycle were overrepresented categories. Moreover, analysis of the small RNA and DNA methylation pathways suggests that distinct mechanisms might be involved in regulating the epigenetic state of the paternal genome. This study has revealed numerous candidate genes whose involvement in sperm cell development and fertilization can now be directly tested.


Calmodulin and the Hypersensitive Response

"Pathogen-associated molecular patterns" (PAMPs) is a relatively new term that describes small molecular motifs consistently found on pathogens. In plants, PAMPs induce the plant hypersensitive response (HR), a type of programmed cell death, characterized by the rapid death of cells in the local region surrounding an infection site. The death of the cells serves to limit the growth and development of the invading pathogen, thereby arresting the progress of disease symptoms caused by the pathogen. Perception of a pathogen or PAMP molecule induces Ca2+ influx across the plasma membrane, leading to cytosolic Ca2+ elevation as an early step in this signaling pathway. A mutant of especial interest in understanding PAMP-induced HR is the dnd1 mutant of Arabidopsis. This mutant lacks a functional plasma membrane Ca2+-conducting cyclic nucleotide-gated channel (CNGC2) and does not undergo HR. Another important signal transduction component is nitric oxide (NO). The fungal PAMP cryptogein and the bacterial PAMP lipopolysaccharide have been shown to elicit NO production in Nicotiana tabacum cell cultures and Arabidopsis leaf cells; in both cases application of a Ca2+ channel blocker or chelation of extracellular Ca2+ prevented PAMP-induced NO generation. The relationship between Ca2+ influx and NO production may be mediated by NO synthase (NOS). Several lines of evidence suggest that the increase in Ca2+ may be upstream of the increase in NO in the HR signal transduction chain. However, the precise mechanism by which the increase in cytosolic Ca2+ is linked to NOS activity and NO generation is unknown. Animal NOS activation is Ca2+/calmodulin (CaM) dependent. The CaM-like protein CML24 has been previously associated with NO-related phenotypes in Arabidopsis. In this issue, Ma et al. (pp. 818–828) report that the HR and its associated increase in NO are both inhibited in loss-of-function cml24-4 mutant plants. PAMP-mediated NO generation in cells of cml24-4 mutants is impaired as well. These findings suggest that Ca2+ influx that occurs early in the HR signal transduction process activates CaM and/or a CML, which in turn induces NO synthesis.


LEC1-Regulated Fatty Acid Biosynthesis

Fatty acids and lipids are major energy reserves in many plant storage tissues, including seeds, as well as essential components of cell membranes and many signal transduction pathways. In Arabidopsis, LEAFY COTYLEDON1 (LEC1) is a key regulator controlling seed maturation. LEC1 is an NFY-B-type or a CCAAT-binding factor-type transcription factor. Both LEC1 and LEC2 (a B3 transcription factor) act as positive regulators upstream of ABSCISIC ACID INSENSITIVE3 (ABI3) and FUSCA3 (FUS3), which in turn function partially redundantly to control the expression of seed storage protein genes. Limited evidence suggests that these four genetic loci are also involved in the regulation of fatty acid metabolism. Mu et al. (pp. 1042–1054) demonstrate that the overexpression of the Arabidopsis LEC1 gene causes globally increased expression of a host of fatty acid biosynthetic genes. In the plastidial fatty acid synthetic pathway, for example, 14 out of 24 enzymes of the pathway are up-regulated in LEC1-overexpressing transgenic plants, including those encoding three subunits of acetyl-CoA carboxylase, a key enzyme controlling the fatty acid biosynthesis flux. Moreover, genes involved in glycolysis and lipid accumulation are also up-regulated. Consistent with these results, the levels of major fatty acid species and lipids were substantially increased in the transgenic plants. Genetic analysis indicates that the LEC1 function is partially dependent on ABI3, FUS3, and WRINKLED1 in the regulation of fatty acid biosynthesis. These results suggest that LEC1, because it is a key regulator of the expression of fatty acid biosynthetic genes, may represent a promising target for the genetic improvement of oil-producing plants.


The Strawberry Fruit Transcriptome

The development of strawberry (Fragaria x ananassa) fruits is accompanied by massive and coordinated changes in the levels of transcripts related to primary and secondary metabolism. Among the major primary metabolites that change during strawberry fruit development are ascorbic acid, amino acids, soluble sugars, and organic acids. The content of sugars and organic acids and the ratios between them play a significant role in the overall flavor of the fruit. In the case of secondary metabolism, phenolic compounds provide the fruit with color, flavor, and protection against pathogenic attack and harsh environmental conditions such as UV exposure. During early stages of fruit development, flavonoids (mainly, condensed tannins) accumulate to high levels, thereby giving immature fruit an astringent flavor. Later in development, when fruit start to ripen, other flavonoids such as anthocyanins and flavonols accumulate to high levels. Moreover, the biosynthesis of hundreds of flavor and aroma compounds occurs during fruit maturation. Nonetheless, a comprehensive view of the changes in strawberry metabolic network across development is lacking. Furthermore, the metabolism of achenes is essentially unexplored, even though achenes contribute significantly to the polyphenol content and stability of strawberry purees. Moreover, the phytochemical resveratrol, present in the achenes of several strawberry cultivars, has become a focus of intense research owing to its dual roles in promoting mammalian longevity and in cancer prevention. By combining GC-MS and LC-MS with the aim of addressing the metabolic regulation underlying fruit-seed development, Fait et al. (pp. 730–750) have constructed a parallel and simultaneous profile of primary and secondary metabolites in both receptacle and achene extracts over the entire course of strawberry development. The results from these analyses suggest that changes in primary and secondary metabolism are specific to the organ and developmental stage. Moreover, during early stages of development, the level of coordinated control across metabolism appeared to be tightly regulated. The comprehensive metabolite analysis presented by these authors sheds light on the metabolic regulation during strawberry development and the different metabolic programs occurring in two functionally distinct organs. The conspicuous differences found between receptacle and achene emphasize the importance in separating the organ-specific events in order to gain a better understanding of strawberry growth, development, and response to environmental cues.

Peter V. Minorsky

Division of Health Professions and Natural Sciences
Mercy College
Dobbs Ferry, New York 10522

FOOTNOTES

www.plantphysiol.org/cgi/doi/10.1104/pp.104.900273


Related articles in Plant Physiol.:

LEAFY COTYLEDON1 Is a Key Regulator of Fatty Acid Biosynthesis in Arabidopsis
Jinye Mu, Helin Tan, Qi Zheng, Fuyou Fu, Yan Liang, Jian Zhang, Xiaohui Yang, Tai Wang, Kang Chong, Xiu-Jie Wang, and Jianru Zuo
Plant Physiol. 2008 148: 1042-1054. [Abstract] [Full Text]  

Nitrate Control of Root Hydraulic Properties in Plants: Translating Local Information to Whole Plant Response
Anna Gorska, Qing Ye, N. Michele Holbrook, and Maciej A. Zwieniecki
Plant Physiol. 2008 148: 1159-1167. [Abstract] [Full Text]  

Comparative Transcriptomics of Arabidopsis Sperm Cells
Filipe Borges, Gabriela Gomes, Rui Gardner, Nuno Moreno, Sheila McCormick, José A. Feijó, and Jörg D. Becker
Plant Physiol. 2008 148: 1168-1181. [Abstract] [Full Text]  

Reconfiguration of the Achene and Receptacle Metabolic Networks during Strawberry Fruit Development
Aaron Fait, Kati Hanhineva, Romina Beleggia, Nir Dai, Ilana Rogachev, Victoria J. Nikiforova, Alisdair R. Fernie, and Asaph Aharoni
Plant Physiol. 2008 148: 730-750. [Abstract] [Full Text]  

Innate Immunity Signaling: Cytosolic Ca2+ Elevation Is Linked to Downstream Nitric Oxide Generation through the Action of Calmodulin or a Calmodulin-Like Protein
Wei Ma, Andries Smigel, Yu-Chang Tsai, Janet Braam, and Gerald A. Berkowitz
Plant Physiol. 2008 148: 818-828. [Abstract] [Full Text]  

The Heme Oxygenase/Carbon Monoxide System Is Involved in the Auxin-Induced Cucumber Adventitious Rooting Process
Wei Xuan, Fu-Yuan Zhu, Sheng Xu, Ben-Kai Huang, Teng-Fang Ling, Ji-Yan Qi, Mao-Bing Ye, and Wen-Biao Shen
Plant Physiol. 2008 148: 881-893. [Abstract] [Full Text]  




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