Dortje Golldack

Tolerance to drought and salt stress in plants: unraveling the signaling networks

Tolerance of plants to abiotic stressors such as drought and salinity is triggered by complex multicomponent signaling pathways to restore cellular homeostasis and promote survival. Major plant transcription factor families such as bZIP, NAC, AP2/ERF, and MYB orchestrate regulatory networks underlying abiotic stress tolerance. Sucrose non-fermenting 1-related protein kinase 2 and mitogen-activated protein kinase pathways contribute to initiation of stress adaptive downstream responses and promote plant growth and development. As a convergent point of multiple abiotic cues, cellular effects of environmental stresses are not only imbalances of ionic and osmotic homeostasis but also impaired photosynthesis, cellular energy depletion, and redox imbalances. Recent evidence of regulatory systems that link sensing and signaling of environmental conditions and the intracellular redox status have shed light on interfaces of stress and energy signaling. ROS (reactive oxygen species) cause severe cellular damage by peroxidation and de-esterification of membrane-lipids, however, current models also define a pivotal signaling function of ROS in triggering tolerance against stress. Recent research advances suggest and support a regulatory role of ROS in the cross talks of stress triggered hormonal signaling such as the abscisic acid pathway and endogenously induced redox and metabolite signals. Here, we discuss and review the versatile molecular convergence in the abiotic stress responsive signaling networks in the context of ROS and lipid-derived signals and the specific role of stomatal signaling.

Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network

Understanding the responses of plants to the major environmental stressors drought and salt is an important topic for the biotechnological application of functional mechanisms of stress adaptation. Here, we review recent discoveries on regulatory systems that link sensing and signaling of these environmental cues focusing on the integrative function of transcription activators. Key components that control and modulate stress adaptive pathways include transcription factors (TFs) ranging from bZIP, AP2/ERF, and MYB proteins to general TFs. Recent studies indicate that molecular dynamics as specific homodimerizations and heterodimerizations as well as modular flexibility and posttranslational modifications determine the functional specificity of TFs in environmental adaptation. Function of central regulators as NAC, WRKY, and zinc finger proteins may be modulated by mechanisms as small RNA (miRNA)-mediated posttranscriptional silencing and reactive oxygen species signaling. In addition to the key function of hub factors of stress tolerance within hierarchical regulatory networks, epigenetic processes as DNA methylation and posttranslational modifications of histones highly influence the efficiency of stress-induced gene expression. Comprehensive elucidation of dynamic coordination of drought and salt responsive TFs in interacting pathways and their specific integration in the cellular network of stress adaptation will provide new opportunities for the engineering of plant tolerance to these environmental stressors.

The Expression of HAK-Type K+ Transporters Is Regulated in Response to Salinity Stress in Common Ice Plant

Four transcripts homologous to K+ transporters of the HAK/KT/KUP family have been characterized from the common ice plant (Mesembryanthemum crystallinum). We report tissue-specific expression of McHAK1 andMcHAK4 transcripts abundant in roots, leaves, and stems.McHAK2 was predominantly present in stems andMcHAK3 in root tissues. By in situ hybridizations, the McHAKs showed signals in the leaf vascular bundles, mesophyll, and epidermal cells as well as in epidermal bladder cells. In mature roots, transcripts were mainly localized to the vasculature, and in differentiated root tips, the strongest signals were obtained from the epidermis. Expression of McHAK1, McHAK2, and McHAK4 complemented a yeast mutant defective in low- and high-affinity K+ uptake. Growth of the yeast mutant was restored at low-millimolar K+ concentrations and was inhibited by Rb+ and Cs+ but was not affected by Na+. Transcript levels of McHAK1 andMcHAK4 increased by K+ starvation and by salt stress of 400 mm NaCl in leaves and roots. Expression of McHAK2 and McHAK3 was stimulated in leaves and was transiently induced in roots in response to high salinity with prestress transcript levels restored in salt-adapted plants. We discuss possible roles for such transporters in ion homeostasis at high salinity.

The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice.

BackgroundPlants respond to extracellularly perceived abiotic stresses such as low temperature, drought, and salinity by activation of complex intracellular signaling cascades that regulate acclimatory biochemical and physiological changes. Protein kinases are major signal transduction factors that have a central role in mediating acclimation to environmental changes in eukaryotic organisms. In this study, we characterized the function of the sucrose nonfermenting 1-related protein kinase2 (SnRK2) SAPK4 in the salt stress response of rice.ResultsTranslational fusion of SAPK4 with the green fluorescent protein (GFP) showed subcellular localization in cytoplasm and nucleus. To examine the role of SAPK4 in salt tolerance we generated transgenic rice plants with over-expression of rice SAPK4 under control of the CaMV-35S promoter. Induced expression of SAPK4 resulted in improved germination, growth and development under salt stress both in seedlings and mature plants. In response to salt stress, the SAPK4-overexpressing rice accumulated less Na+ and Cl- and showed improved photosynthesis. SAPK4-regulated genes with functions in ion homeostasis and oxidative stress response were identified: the vacuolar H+-ATPase, the Na+/H+ antiporter NHX1, the Cl- channel OsCLC1 and a catalase.ConclusionOur results show that SAPK4 regulates ion homeostasis and growth and development under salinity and suggest function of SAPK4 as a regulatory factor in plant salt stress acclimation. Identification of signaling elements involved in stress adaptation in plants presents a powerful approach to identify transcriptional activators of adaptive mechanisms to environmental changes that have the potential to improve tolerance in crop plants.

The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance.

Soil salinity severely affects plant growth and agricultural productivity. AtbZIP24 encodes a bZIP transcription factor that is induced by salt stress in Arabidopsis thaliana but suppressed in the salt-tolerant relative Lobularia maritima. Transcriptional repression of AtbZIP24 using RNA interference improved salt tolerance in A. thaliana. Under non-stress growth conditions, transgenic A. thaliana lines with decreased AtbZIP24 expression activated the expression of stress-inducible genes involved in cytoplasmic ion homeostasis and osmotic adjustment: the Na(+) transporter AtHKT1, the Na(+)/H(+) antiporter AtSOS1, the aquaporin AtPIP2.1, and a glutamine synthetase. In addition, candidate target genes of AtbZIP24 with functions in plant growth and development were identified such as an argonaute (AGO1)-related protein and cyclophilin AtCYP19. The salt tolerance in transgenic plants correlated with reduced Na(+) accumulation in leaves. In vivo interaction of AtbZIP24 as a homodimer was shown using fluorescence energy transfer (FRET) with cyan fluorescent protein (CFP) and yellow fluorescent protein (YFP) as fused FRET pairs. Translational fusion of AtbZIP24 with GFP showed subcellular localization of the protein in nucleus and cytoplasm in plants grown under control conditions whereas in response to salt stress AtbZIP24 was preferentially targeted to the nucleus. It is concluded that AtbZIP24 is an important regulator of salt stress response in plants. The modification of transcriptional control by regulatory transcription factors provides a useful strategy for improving salt tolerance in plants.

New Insight into the Structure and Regulation of the Plant Vacuolar H+-ATPase

Plant cells are characterized by a highly active secretory system that includes the large central vacuole found in most differentiated tissues. The plant vacuolar H+-ATPase plays an essential role in maintaining the ionic and metabolic gradients across endomembranes, in activating transport processes and vesicle dynamics, and, hence, is indispensable for plant growth, development, and adaptation to changing environmental conditions. The review summarizes recent advances in elucidating the structure, subunit composition, localization, and regulation of plant V-ATPase. Emerging knowledge on subunit isogenes from Arabidopsis and rice genomic sequences as well as from Mesembryanthemum illustrates another level of complexity, the regulation of isogene expression and function of subunit isoforms. To this end, the review attempts to define directions of future research on plant V-ATPase.

Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress.

Abiotic stresses resulting from water deficit, high salinity or periods of drought adversely affect plant growth and development and represent major selective forces during plant evolution. The raffinose family oligosaccharides (RFOs) are synthesised from sucrose by the subsequent addition of activated galactinol moieties donated by galactinol. RFOs are characterised as compatible solutes involved in stress tolerance defence mechanisms, although evidence also suggests that they act as antioxidants, are part of carbon partitioning strategies and may serve as signals in response to stress. The key enzyme and regulatory point in RFO biosynthesis is galactinol synthase (GolS), and an increase of GolS in expression and activity is often associated with abiotic stress. It has also been shown that different GolS isoforms are expressed in response to different types of abiotic stress, suggesting that the timing and accumulation of RFOs are controlled for each abiotic stress. However, the accumulation of RFOs in response to stress is not universal and other functional roles have been suggested for RFOs, such as being part of a carbon storage mechanism. Transgenic Arabidopsis plants with increased galactinol and raffinose concentrations had better ROS scavenging capacity, while many sugars have been shown in vitro to have antioxidant activity, suggesting that RFOs may also act as antioxidants. The RFO pathway also interacts with other carbohydrate pathways, such as that of O-methyl inositol (OMI), which shows that the functional relevance of RFOs must not be seen in isolation to overall carbon re-allocation during stress responses.

Mutation of the matrix metalloproteinase At2-MMP inhibits growth and causes late flowering and early senescence in Arabidopsis.

This study characterizes the expression and functional significance of the member of the matrix metalloproteinase (MMP) family At2-MMP from Arabidopsis. By transcript analysis, expression of At2-MMP was found in leaves and roots of juvenile Arabidopsis and leaves, roots, and inflorescences of mature flowering plants showing strong increase of transcript abundance with aging. Cell specificity of expression of At2-MMP was studied by in situ hybridizations in leaves and flowers of Arabidopsis. In leaves, the gene was expressed in the phloem, in developing xylem elements, epidermal cells, and neighboring mesophyll cell layers. In flowers, signals were localized in pistils, ovules, and receptacles. In anArabidopsis mutant (at2-mmp-1) carrying a tDNA insertion in At2-MMP, neither germination nor development of plants was modified in comparison to the wild type in the juvenile rosette stage. Starting with the onset of shoots, growth of roots, leaves, and shoots was inhibited compared with the wild type, and the plants were characterized by late flowering. Besides the flowering, at2-mmp-1 plants showed fast degradation of chlorophyll in leaves and early senescence. These results demonstrate the involvement of At2-MMP in plant growth, morphogenesis, and development with particular relevance for flowering and senescence.

Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorable conditions

Plants adapt to adverse environments by integrating growth and development to environmentally activated cues. Within the adaptive signaling networks, plant hormones tightly control convergent developmental and stress adaptive processes and coordinate cellular responses to external and internal conditions. Recent studies have uncovered novel antagonizing roles of the plant hormones gibberellin (GA) and abscisic acid (ABA) in integrating growth and development in plants with environmental signaling. According to current concepts, GRAS transcription factors of the DELLA and SCARECROW-LIKE (SCL) types have a key role as major growth regulators and have pivotal functions in modulating GA signaling. Significantly, current models emphasize a function of DELLA proteins as central regulators in GA homeostasis. DELLA proteins interact with the cellular GA receptor GID1 (GA-INSENSITIVE DWARF1) and degradation of DELLAs activates the function of GA. Supplementary to the prevailing view of a pivotal role of GRAS family transcriptional factors in plant growth regulation, recent work has suggested that the DELLA and SCL proteins integrate generic GA responses into ABA-controlled abiotic stress tolerance. Here, we review and discuss how GRAS type proteins influence plant development and versatile adaptation as hubs in GA and ABA triggered signaling pathways.

Salt-induced expression of NADP-dependent isocitrate dehydrogenase and ferredoxin-dependent glutamate synthase in Mesembryanthemum crystallinum

Abstract. NADP-specific isocitrate dehydrogenase is a key cytosolic enzyme that links C and N metabolism by supplying C skeletons for primary N assimilation in plants. We report the characterization of the transcript Mc-ICDH1 encoding an NADP-dependent isocitrate dehydrogenase (NADP-ICDH, EC 1.1.1.42) from the facultative halophyte Mesembryanthemum crystallinum L., focussing on salt-dependent regulation of the enzyme. The activity of NADP-ICDH in plants adapted to high salinity increased in leaves and decreased in roots. By transcript analyses and Western-type hybridizations, expression of Mc-ICDH1 was found to be stimulated in leaves in salt-adapted M. crystallinum. By immunocytological analyses, NADP-ICDH proteins were localized to most cell types with strongest expression in epidermal cells and in the vascular tissue. In leaves of salt-adapted plants, signal intensities increased in mesophyll cells. In contrast to Mc-ICDH1, the activity and transcript abundance of ferredoxin-dependent glutamate synthase (Fd-GOGAT, EC 1.4.7.1), which is the key enzyme of N assimilation and biosynthesis of amino acids, decreased in leaves in response to salt stress. The physiological roles of NADP-ICDH and Fd-GOGAT in the adaptation of plants to high salinity are discussed.