A Special Issue on Plant Stress Biology: From Model Species to Crops

Abstract

As sessile organisms, the growth and productivity of land plants are continuously confronted with a variety of biotic and abiotic stresses. As a consequence, land plants have evolved a set of perception and signaling mechanisms to respond or adapt to adverse environmental conditions via regulation of transcription and gene expression, fine-tuning protein translation, modification and degradation, and metabolic reprogramming. Understanding the stress signaling pathways as well as the molecular and physiological mechanisms underlying stress tolerance in plants is not only fundamental for plant biology research, but also pivotal for practical applications such as genetic improvement of crops. Undoubtedly, the findings in the model species such as Arabidopsis thaliana and rice in the past two decades have greatly advanced our understanding on plant stress biology, whereas the distinct mechanisms by which certain crop and emerging model plants employ to survive under stresses are being extensively studied. In this context, Molecular Plant published a special issue on ‘Plant Stress Biology’ (Volume 6, Number 2, 2013), which has been freely accessible online since March 2014. This special issue, organized by Drs Hans Bohnert, Ray Bressan, and Jian-Kang Zhu, collected one research highlight, three reviews, and 13 research articles. The research highlight by de Zelicourt et al., 2013de Zelicourt A. Al-Yousif M. Hirt H. Rhizosphere microbes as essential partners for plant stress tolerance.Mol. Plant. 2013; 6: 242-245Abstract Full Text Full Text PDF PubMed Scopus (157) Google Scholar conducted an up-to-date analysis of the known roles of rhizosphere microbes, with a focus on the non-symbiotic bacteria and fungi in plant stress tolerance, and highlighted the usefulness of beneficial microbes in improving plant stress tolerance (de Zelicourt et al., 2013de Zelicourt A. Al-Yousif M. Hirt H. Rhizosphere microbes as essential partners for plant stress tolerance.Mol. Plant. 2013; 6: 242-245Abstract Full Text Full Text PDF PubMed Scopus (157) Google Scholar). Pamela Ronald and colleagues (2013) reviewed the recent advances in dissecting the crosstalk mechanisms between biotic and abiotic stress-responsive signaling pathways in rice. By highlighting the systems biology approaches for analyzing stress-regulatory networks, they discussed the crosstalk of signaling pathways mediated by three important regulators: XA21 which encodes a receptor kinase conferring resistance to Xanthomonas oryzae pv. oryzae, NH1 which is a key regulator of systemic acquired resistance, and SUB1A encoding an ethylene-responsive transcription factor crucial for tolerance to submergence stress (Sharma et al., 2013Sharma R. De Vleesschauwer D. Sharma M.K. Ronald P.C Recent advances in dissecting stress-regulatory crosstalk in rice.Mol. Plant. 2013; 6: 250-260Abstract Full Text Full Text PDF PubMed Scopus (128) Google Scholar). As plant-specific transcription factors, members of the WRKY gene family play diverse roles in plant growth and development, and especially are critical for plant responses to biotic and abiotic stresses. The review by Chae et al., 2013Chae H.B. Moon J.C. Shin M.R. Chi Y.H. Jung Y.J. Lee S.Y. Nawkar G.M. Jung H.S. Hyun J.K. Kim W.Y. et al.Thioredoxin reductase type c (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function.Mol. Plant. 2013; 6: 323-336Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar summarized the recent findings of protein–protein interaction studies on WRKY transcription factors and discussed the regulatory roles and action mode of the interacting partners in the WRKY signaling networks (Chi et al., 2013Chi Y.J. Yang Y. Zhou Y. Zhou J. Fan B. Yu J.Q. Chen Z. Protein-protein interactions in the regulation of WRKY transcription factors.Mol. Plant. 2013; 6: 287-300Abstract Full Text Full Text PDF PubMed Scopus (225) Google Scholar). Salinity stress is a major environmental constraint to agricultural plant productivity, as it affects the production in over 30% of irrigated crops and 7% of dryland agriculture worldwide (Schroeder et al., 2013Schroeder J.I. Delhaize E. Frommer W.B. Guerinot M.L. Harrison M.J. Herrera-Estrella L. Horie T. Kochian L.V. Munns R. Nishizawa N.K. et al.Using membrane transporters to improve crops for sustainable food production.Nature. 2013; 497: 60-66Crossref PubMed Scopus (347) Google Scholar). The Salt-Overly-Sensitive (SOS) signaling pathway has been discovered to play crucial roles in modulating cellular ion homeostasis in response to salinity stress to confer plants with salt tolerance. In Arabidopsis, after perception of salinity stress, a Ca2+ spike signal is sensed by SOS3 and SOS3-like (SCaBP8/CBL10) calcium sensors, which form a complex with SOS2 protein kinase at the plasma membrane to activate the SOS1, a Na+/H+ transporter, leading to subsequent extrusion of excessive Na+ from the cytosol. Ji et al., 2013Ji H.T. Pardo J.M. Batelli G. Van Oosten M.J. Bressan R.A. Li X. The Salt Overly Sensitive (SOS) pathway: established and emerging roles.Mol. Plant. 2013; 6: 275-286Abstract Full Text Full Text PDF PubMed Scopus (409) Google Scholar reviewed the known and emerging roles of the SOS pathway, focusing on the emerging complexity of the SOS signaling and SOS proteins. Novel cellular functions of SOS proteins in regulating cellular cytoskeleton dynamics and root architecture as well as the crosstalk with other signaling pathways were critically discussed (Ji et al., 2013Ji H.T. Pardo J.M. Batelli G. Van Oosten M.J. Bressan R.A. Li X. The Salt Overly Sensitive (SOS) pathway: established and emerging roles.Mol. Plant. 2013; 6: 275-286Abstract Full Text Full Text PDF PubMed Scopus (409) Google Scholar). Recent evidence also strongly implicates that plants utilize more complex mechanisms to respond to salinity. For example, members of the HKT (high-affinity potassium transporter) gene family that comprises Na+ and Na+/K+ transporters have been revealed to mediate salt tolerance in diverse plant species. Arabidopsis HKT1;1 functions to mediate Na+ exclusion from leaves and unload Na+ from xylem vessels in the root. Hill et al., 2013Hill C.B. Jha D. Bacic A. Tester M. Roessner U. Characterization of ion contents and metabolic responses to salt stress of different Arabidopsis AtHKT1;1 genotypes and their parental strains.Mol. Plant. 2013; 6: 350-368Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar reported a study on the profiling of metabolites and element nutrients in the shoots and roots of different AtHKT1;1 knockout and overexpression lines before and after salinity stress. By correlation analysis, they identified associations between the Na+ content and some metabolites, including several sugars, suggesting that metabolic regulation is important for plant responses to salinity stress (Hill et al., 2013Hill C.B. Jha D. Bacic A. Tester M. Roessner U. Characterization of ion contents and metabolic responses to salt stress of different Arabidopsis AtHKT1;1 genotypes and their parental strains.Mol. Plant. 2013; 6: 350-368Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar). Ca2+ signaling regulates multiple cellular responses to abiotic and biotic stresses as well as developmental cues. To dissect the Ca2+ signaling mechanisms, a reliable approach is needed to accurately measure the cellular Ca2+ dynamics in plants. Guan et al., 2013Guan Q.M. Wen C.L. Zeng H.T. Zhu J.H A KH domain-containing putative RNA-binding protein is critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis.Mol. Plant. 2013; 6: 386-395Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar developed an Aequorin-based Film Adhesive Seedling (FAS) luminescence recording system that allows the sensitive and tissue-specific monitoring of Ca2+ dynamics in response to various stimuli in Arabidopsis. Exploiting this system, they revealed stimulus- and tissue-specific Ca2+ signatures in Arabidopsis seedlings that are associated with the type and strength of stimuli (Zhu et al., 2013Zhu X.H. Feng Y. Liang G.M. Liu N. Zhu J.K Aequorin-based luminescence imaging reveals stimulus- and tissue-specific Ca2+ dynamics in Arabidopsis plants.Mol. Plant. 2013; 6: 444-455Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar). Both Ca2+ and reactive oxygen species (ROS) are critical second messengers signaling developmental and environmental cues. Drerup et al., 2013Drerup M.M. Schlücking K. Hashimoto K. Manishankar P. Steinhorst L. Kuchitsu K. Kudla J. The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase cipk26 regulate the Arabidopsis NADPH oxidase RBOHF.Mol. Plant. 2013; 6: 559-569Abstract Full Text Full Text PDF PubMed Scopus (276) Google Scholar reported that protein kinase CIPK26, a partner of Ca2+ sensor proteins CBL1 and CBL9, could specifically interact with and phosphorylate RBOHF, one of NADPH oxidases producing ROS. Co-expression of CBL1 or CBL9 with CIPK26 enhanced ROS production by RBOHF in human cells, suggesting a direct crosstalk between CBL–CIPK-mediated Ca2+ signaling and ROS signaling in plants (Drerup et al., 2013Drerup M.M. Schlücking K. Hashimoto K. Manishankar P. Steinhorst L. Kuchitsu K. Kudla J. The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase cipk26 regulate the Arabidopsis NADPH oxidase RBOHF.Mol. Plant. 2013; 6: 559-569Abstract Full Text Full Text PDF PubMed Scopus (276) Google Scholar). High temperature and drought are two other important abiotic stresses that affect plant growth and productivity. Several studies in this issue centered on the molecular analyses of plant responses to heat stress. Popova et al., 2013Popova O.V. Dinh H.Q. Aufsatz W. Jonak C. The RdDM pathway is required for basal heat tolerance in Arabidopsis.Mol. Plant. 2013; 6: 396-410Abstract Full Text Full Text PDF PubMed Scopus (120) Google Scholar showed that the RNA-dependent DNA methylation pathway is involved in basal heat-stress tolerance in Arabidopsis (Popova et al., 2013Popova O.V. Dinh H.Q. Aufsatz W. Jonak C. The RdDM pathway is required for basal heat tolerance in Arabidopsis.Mol. Plant. 2013; 6: 396-410Abstract Full Text Full Text PDF PubMed Scopus (120) Google Scholar). Guan et al., 2013Guan Q.M. Wen C.L. Zeng H.T. Zhu J.H A KH domain-containing putative RNA-binding protein is critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis.Mol. Plant. 2013; 6: 386-395Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar identified RCF3, a KH domain-containing RNA-binding protein localized in the nucleus, as an upstream negative regulator of thermotolerance by modulating the expression of genes encoding heat-shock proteins (HSPs) in Arabidopsis (Guan et al., 2013Guan Q.M. Wen C.L. Zeng H.T. Zhu J.H A KH domain-containing putative RNA-binding protein is critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis.Mol. Plant. 2013; 6: 386-395Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). Thellungiella salsuginea is a close relative of Arabidopsis but is more tolerant not only to salinity, but also to several other abiotic stresses, including high temperature as demonstrated by Higashi et al., 2013Higashi Y. Ohama N. Ishikawa T. Katori T. Shimura A. Kusakabe K. Yamaguchi-Shinozaki K. Ishida J. Tanaka M. Seki M. et al.HsfA1d, a protein identified via fox hunting using Thellungiella salsuginea cDNAs improves heat tolerance by regulating heat-stress-responsive gene expression.Mol. Plant. 2013; 6: 411-422Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar. Using the full-length cDNA overexpressing (FOX) gene hunting approach, Higashi et al., 2013Higashi Y. Ohama N. Ishikawa T. Katori T. Shimura A. Kusakabe K. Yamaguchi-Shinozaki K. Ishida J. Tanaka M. Seki M. et al.HsfA1d, a protein identified via fox hunting using Thellungiella salsuginea cDNAs improves heat tolerance by regulating heat-stress-responsive gene expression.Mol. Plant. 2013; 6: 411-422Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar identified that TsHsfA1d, a gene encoding a heat-shock transcription factor, could confer markedly enhanced heat tolerance when overexpressed in Arabidopsis. Both TsHsfA1d- and AtHsfA1d-overexpressing plants exhibited enhanced heat tolerance and up-regulated expression of many heat-stress-responsive genes, suggesting that HsfA1 is potentially useful for engineering the heat tolerance in crop plants (Higashi et al., 2013Higashi Y. Ohama N. Ishikawa T. Katori T. Shimura A. Kusakabe K. Yamaguchi-Shinozaki K. Ishida J. Tanaka M. Seki M. et al.HsfA1d, a protein identified via fox hunting using Thellungiella salsuginea cDNAs improves heat tolerance by regulating heat-stress-responsive gene expression.Mol. Plant. 2013; 6: 411-422Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar). Chae et al., 2013Chae H.B. Moon J.C. Shin M.R. Chi Y.H. Jung Y.J. Lee S.Y. Nawkar G.M. Jung H.S. Hyun J.K. Kim W.Y. et al.Thioredoxin reductase type c (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function.Mol. Plant. 2013; 6: 323-336Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar reported that overexpression of NADPH-thioredoxin reductase type C (NTRC) in Arabidopsis resulted in enhanced thermotolerance, whereas NTRC knockout mutant plants exhibited a temperature-sensitive phenotype. Although NTRC has multiple functions, mutagenesis analysis suggested that heat-shock-dependent and redox-regulated holdase chaperone activity of NTRC is responsible for conferring plants with the enhanced thermotolerance (Chae et al., 2013Chae H.B. Moon J.C. Shin M.R. Chi Y.H. Jung Y.J. Lee S.Y. Nawkar G.M. Jung H.S. Hyun J.K. Kim W.Y. et al.Thioredoxin reductase type c (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function.Mol. Plant. 2013; 6: 323-336Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar). Two research articles presented the studies regarding the effects of drought stress on Brachypodium distachyon, an emerging model species for monocot cereal crops such as wheat, barley, and rye. By developing a reproducible in vivo drought assay, Bertolini et al., 2013Bertolini E. Verelst W. Horner D.S. Gianfranceschi L. Piccolo V. Inzé D. Pè M.E. Mica E. Addressing the role of microRNAs in reprogramming leaf growth during drought stress in Brachypodium distachyon.Mol. Plant. 2013; 6: 423-443Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar investigated the effect of growth-limiting drought stress on B. distachyon leaf development, and found that drought stress inhibits B. distachyon leaf growth mainly by decreasing cell expansion. Transcriptome analysis suggests the molecular response of B. distachyon leaves to drought strongly depends on the leaf developmental stage (Verelst et al., 2013Verelst W. Bertolini E. De Bodt S. Vandepoele K. Demeulenaere M. Pè M.E. Inzé D. Molecular and physiological analysis of growth-limiting drought stress in Brachypodium distachyon leaves.Mol. Plant. 2013; 6: 311-322Abstract Full Text Full Text PDF PubMed Scopus (86) Google Scholar). With the same in vivo drought assay and by high-throughput sequencing of small RNAs (sRNAs) from B. distachyon leaves, Bertolini et al., 2013Bertolini E. Verelst W. Horner D.S. Gianfranceschi L. Piccolo V. Inzé D. Pè M.E. Mica E. Addressing the role of microRNAs in reprogramming leaf growth during drought stress in Brachypodium distachyon.Mol. Plant. 2013; 6: 423-443Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar presented a profiling study of the known and newly discovered miRNAs in drought response and leaf development of B. distachyon. A number of miRNAs were found to be involved in developmental reprogramming of leaf growth in response to drought (Bertolini et al., 2013Bertolini E. Verelst W. Horner D.S. Gianfranceschi L. Piccolo V. Inzé D. Pè M.E. Mica E. Addressing the role of microRNAs in reprogramming leaf growth during drought stress in Brachypodium distachyon.Mol. Plant. 2013; 6: 423-443Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar). As one of the two surviving lineages of vascular plants, Selaginella species in the spikemoss family, Selaginellaceae, are emerging as model systems for understanding the evolution of multiple traits of vascular plants. S. lepidophylla is one of a few species of spikemosses that have evolved the well-known ability to survive almost complete desiccation: its microphylls curl to form a tight ball under dry conditions but displays fully expanded green microphylls when hydrated. In this issue, Yobi et al., 2013Yobi A. Wone B.W.M. Xu W. Alexander D.C. Guo L. Ryals J.A. Oliver M.J. Cushman J.C Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance.Mol. Plant. 2013; 6: 369-385Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar reported a metabolomic profiling study towards providing the mechanistic understanding of desiccation tolerance in S. lepidophylla (Yobi et al., 2013Yobi A. Wone B.W.M. Xu W. Alexander D.C. Guo L. Ryals J.A. Oliver M.J. Cushman J.C Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance.Mol. Plant. 2013; 6: 369-385Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar). Drought stress can induce abscisic acid (ABA) accumulation in guard cells to trigger stomatal closure. SLAC1, an outward anion channel, is required for stomatal closure induced by ABA through reversible regulation of protein phosphorylation involving ABA signaling components, protein phosphatase 2C (PP2C) members, and an SnRK-type kinase OST1/SnRK2.6. In another work, Chae et al., 2013Chae H.B. Moon J.C. Shin M.R. Chi Y.H. Jung Y.J. Lee S.Y. Nawkar G.M. Jung H.S. Hyun J.K. Kim W.Y. et al.Thioredoxin reductase type c (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function.Mol. Plant. 2013; 6: 323-336Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar reconstituted the ABA signaling pathway as a protein–protein interaction relay from the PYL/RCAR-type ABA receptors to the PP22C–SnRK2 phosphatase-kinase pairs that interact with and regulate the channel activity of SLAC1 in guard cells (Lee et al., 2013Lee S.C. Lim C.W. Lan W.Z. He K. Luan S. ABA signaling in guard cells entails a dynamic protein–protein interaction relay from the PYL–RCAR family receptors to ion channels.Mol. Plant. 2013; 6: 528-538Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar). Finally, two research articles reported the findings with values for practical applications. Chae et al., 2013Chae H.B. Moon J.C. Shin M.R. Chi Y.H. Jung Y.J. Lee S.Y. Nawkar G.M. Jung H.S. Hyun J.K. Kim W.Y. et al.Thioredoxin reductase type c (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function.Mol. Plant. 2013; 6: 323-336Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar showed that transgenic potato constitutively overexpressing Arabidopsis AtYUC6, a gene of the YUCCA family of flavin monooxygenases that catalyze the synthesis of active auxin, displayed high-auxin phenotypes as well as enhanced drought tolerance, suggesting that manipulation of auxin biosynthesis pathway may improve crop plants with enhanced tolerance to drought (Kim et al., 2013Kim J.I. Baek D. Park H.C. Chun H.J. Oh D.H. Lee M.K. Cha J.Y. Kim W.Y. Kim M.C. Chung W.S. et al.Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit.Mol. Plant. 2013; 6: 337-349Abstract Full Text Full Text PDF PubMed Scopus (131) Google Scholar). Interestingly, another report links the molecular and physiological researches with the field control of citrus disease. By profiling sRNAs in citrus trees, Zhao et al., 2013Zhao H.W. Sun R.B. Albrecht U. Padmanabhan C. Wang A.R. Coffey M.D. Girke T. Wang Z.H. Close T.J. Roose M. et al.Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus Huanglongbing disease.Mol. Plant. 2013; 6: 301-310Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar found that, in addition to several other sRNAs, miR399, which is induced by phosphate starvation to regulate its homeostasis in Arabidopsis, was induced specifically by Huanglongbing (HLB), a destructive disease in citrus. Furthermore, phosphorus deficiency was uncovered to be associated with the HLB-infected citrus, and applying phosphorus solutions to HLB-positive trees could reduce HLB symptom severity and significantly improve fruit production in a 3-year field trial, providing a potential approach for managing citrus HLB disease (Zhao et al., 2013Zhao H.W. Sun R.B. Albrecht U. Padmanabhan C. Wang A.R. Coffey M.D. Girke T. Wang Z.H. Close T.J. Roose M. et al.Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus Huanglongbing disease.Mol. Plant. 2013; 6: 301-310Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar). In short, this collection of outstanding reviews and research articles might have substantially increased our knowledge about stress signaling and response mechanisms in plants from model species to certain crops. An increasing number of studies are being conducted in the emerging model species towards elucidating their unique and distinct aspects in response to stresses. Efforts are also being made to translate the gained knowledge into innovative applications in agriculture. These would be new focuses of future studies in the field. We hope now this FREE accessible issue will stimulate more discussions and studies that help in guiding the research on plant stress biology into a new era.