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Cell Cycle Regulation in the Plant Response to Stress

Feifei Qi, Fuxin Zhang

Frontiers in Plant Science · 2020 · Review · CC BY

doi:10.3389/fpls.2019.01765

Abstract

As sessile organisms, plants face a variety of environmental challenges. Their reproduction and survival depend on their ability to adapt to these stressors, which include water, heat stress, high salinity, and pathogen infection. Failure to adapt to these stressors results in programmed cell death and decreased viability, as well as reduced productivity in the case of crop plants. The growth and development of plants are maintained by meiosis and mitosis as well as endoreduplication, during which DNA replicates without cytokinesis, leading to polyploidy. As in other eukaryotes, the cell cycle in plants consists of four stages (G1, S, G2, and M) with two major check points, namely, the G1/S check point and G2/M check point, that ensure normal cell division. Progression through these checkpoints involves the activity of cyclin-dependent kinases and their regulatory subunits known as cyclins. In order for plants to survive, cell cycle control must be balanced with adaption to dynamic environmental conditions. In this review, we summarize recent advances in our understanding of cell cycle regulation in plants, with a focus on the molecular interactions of cell cycle machinery in the context of stress tolerance.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

All organisms have evolved mechanisms to cope with a broad range of biotic and abiotic stresses. The former is caused by external organisms such as bacteria, virus, fungi, and animals, whereas the latter is attributable to environmental conditions, such as drought, cold temperature, changes in salinity, and so on. Unlike animals, plants are sessile and have therefore developed unique stress responses involving many types of sensor that ensure their survival.

In nature, plants are vulnerable to pathogens and predators. The immune system in animals has innate and adaptive components; immune signaling cascades have been widely studied in fish, cow, pig, and mouse. In contrast, plants lack the adaptive component and rely primarily on two layers of innate immunity in their response to pathogen infection. Plants sense pathogens through recognition of conserved microbe-associated molecular patterns and host-derived damage-associated molecular patterns. Additionally, disease resistance proteins recognize effector molecules secreted by pathogens and induce a more robust and rapid immune response that usually leads to programmed cell death. However, immune activation perturbs the cell cycle, which controls plant growth; recent evidence suggests a close connection between cell cycle kinetics and immunity in plants.

Plants can detect various environmental signals such as high salt concentration, cold temperature, reactive oxygen species levels, waterlogging, phosphate scarcity, and ultraviolet (UV) radiation. Failure to appropriately respond to these stressors decreases plant productivity and affects human food and animal feed supplies. As such, considerable effort has been invested in developing methods to improve stress resistance in crop plants such as wheat, peanut, rice, tobacco, tomato, maize, cotton, and bean.

Plants growth results from the coordinated interaction of mitotic cell cycle and cell expansion. As in animals, the plant cell cycle consists of four distinct phases: G1 (postmitotic interphase), S (DNA synthesis phase), G2 (premitotic interphase), and M (mitosis/cytokinesis). Cell cycle progression is driven by cyclin-dependent kinases (CDKs) which cooperated with cyclins. There are seven classes of cyclins in plants which consists of approximately 60 cyclin genes. Among them, we know more about the A, B, and D classes. In general, D-type cyclins are considered as the regulators of G1-to-S transition, A-type cyclins are thought to control S-to-M phase, and B-type cyclins control G2-to-M transition. At G1-to-S transition, CDKA/CYCD complex phosphorylates the retinoblastoma-related (RBR) protein which activates the S-phase transcription factor, “E2F”. E2Fs promotes the G1–S transition by modulating the expression of genes involved in DNA replication, cell-cycle progression and chromatin dynamics. The negative regulation of G1/S transition is the KRPs (Kip-related proteins) and SIM (SIAMESE) which play roles as the inhibitors of CDKA/CYCD complex. At G2/M transition, CDKA and CDKB bind to CYCA, CYCB, or CYCD and drive cells into division. Meanwhile, the activities of CDKA and CDKB are negatively regulated by the WEE1 kinase. The CDC25 homologous kinase, which dephosphorylates the inhibitory phosphorylated site in CDK, still needs to be identified. Once the CDK/CYC complexes are activated, they trigger the G2-to-M transition through phosphorylating numerous of different substrates. Mitotic exit requires the proteolytic degradation of the cyclin subunits which mediated by the anaphase-promoting complex (APC) ( Figure 1 ). Although the basic mechanisms which control mitotic cell cycle progression are conserved from plants to vertebrate, plants have unique molecules orchestrating the cell cycle. Moreover, plants have usually a variety of cyclins even though the function of many of which is unclear. At the same time, plants don’t have Cyclin E, which is a major target for organ regulators in animals.

In addition to mitotic cell cycle, the endocycle plays pivotal role in plant growth. Endocycle means that DNA replication in the absence of cytokinesis and leads to polyploid. The switch from the mitotic cell cycle to the endocycle involves changes in the regulation and abundance of a wide broad of cyclin-dependent kinases (CDKs), cyclins (CYC), and regulatory proteins/transcription factors. Endopolyploidy is common in reproductive tissues of plants, for example the nutritive tissue of the endosperm in seeds. The onset of endopolyploidy is induced in some cell tissues in response to stress. In this review, we summarize the molecular link between environmental signals and cell cycle progression and the stress response in plants.

Cell Cycle Regulation and Immunity

All animals and plants are vulnerable to infection with viruses and bacteria. For example, cattle and pigs are easily infected with bovine ephemeral fever virus and porcine circovirus, respectively, and rely on innate and adaptive immunity for protection. The bacterial strain BGI-1, isolated from the gut of the German cockroach (Blattella germanica), contributes to anti-entomopathogenic fungal infection. Additionally, pathogenic microorganism invasion induces the innate immune responses in zebrafish. Toll-like receptor (TLR)22, TLR18, X box-binding protein 1, and interferon regulatory factor 1 have been identified as critical molecules involved in immunity in the common carp. However, unlike animals, plants lack a somatic adaptive immune system and instead rely on the innate immunity of each cell to detect signals originating from sites of infection. Plants detect the extracellular pathogens through plasma membrane-localized pattern recognition receptors (PRRs) that recognize conserved microbe-associated molecular patterns (MAMPs), such as bacterial flg22 and elf18 (active epitopes of bacterial flagellin and elongation factor-Tu, respectively), and then drive patterns-triggered immunity (PTI). In addition, plants possess a variety of resistance (R) genes which encode proteins containing nucleotide binding (NB) and leucine rich repeat (LRR) domains. NB-LRR proteins induce effector-triggered immunity (ETI) after specific perception of pathogenic T3SEs.

Interaction with pathogens influences cell cycle progression in plants. In Arabidopsis thaliana, Cabbage leaf curl virus infection alters the expression of cell cycle-related factors; overexpression of CYCD3;1 or E2FB, both of which promote mitosis, increases polyploidy and strongly inhibits Cabbage leaf curl virus infection. Powdery mildew (PM), which is the main pathogen of cereal crops, stimulates the endocycle and increases calcium signaling at the infection site in Arabidopsis. The loss-of-function mutant of MYB3R4, a transcription factor required for endocycle initiation, suppresses PM growth. However, it’s currently unclear how cell immunity response is communicated to cell cycle progression.

In a broad sense, PTI functions through several pathways such as the hormone pathways or the phosphorylation of mitogen-activated protein kinases (MAPKs) or the rapid production of reactive oxygen species (ROS) and Ca2+-mediated activation of Ca2+-dependent kinases (CDPKs) that activate transcription factors to induce the expression of down-stream genes. Immunity-triggered growth inhibition might be partly related to jasmonates (JA)-mediated inhibition of the cell cycle. Increased JA level is a positive defense response to pathogen infection. indicated that JA suppressed CDKA;1 and CYCB1;1. Recent studies have further revealed that JA signaling stabilizes DELLA proteins which induce the CDKA and CDKB inhibitors KRP2, SIM, and SMR. Therefore, inhibited cell cycle progression may be a consequence of hormone. Harnessing the toxic properties of reactive oxygen species (ROS) to fight against invading pathogens might be another reason for prolonged cell cycle. ROS in adequate concentration directs the invaded plant cells towards apoptosis so as to restrict the fungal infection spread. In mammalian cells, ROS influence cell cycle progression via phosphorylation and ubiquitination of CDKs and cell cycle regulatory molecules, such as CKI and Cdc25. ROS exert their effect on Cdc25 activity via enhancing phosphorylation of Cdc25 or alternatively inactivation of Cdc25 by sulfonation of cysteine in the active site. Therefore, it’s reasonable to speculate plant ROS play roles in the similar ways as in mammalian. Regardless of pathogen type, ETI is commonly accompanied by programmed cell death (PCD) at the infection site to stop pathogen spread.

It’s of significant importance to investigate whether cell cycle regulatory genes promote immunity positively. The Arabidopsis genes OMISSION OF THE SECOND DIVISION (OSD)1 and its homolog UV-B-INSENSITIVE (UVI)4 negatively regulate the activities of anaphase-promoting complex (APC)/cyclosome. Overexpression of both OSD1 and UVI4, or APC6 deficiency, enhances immunity to pathogens by stimulating the expression of disease resistance genes, such as SNC1, which is associated with inhibition of the endocycle. However, the mechanisms by which OSD1 and UVI4 enhance immunity still need to be explored. In fact, recent studies indicated a direct link of cell cycle regulators in immunity, for example, TEOSINTE BRANCHED1, CYCLOIDEA, PCF1 (TCP)15, and MODIFIER OF SNC1 (MOS1). As a transcription factor, TCP15 regulates the transcription of CYCA2;3 and SUPPRESSOR OF rps4-RLD1, which encodes a protein that negatively regulates plant immunity. In Arabidopsis, MOS1 directly interacts with TCP15, and affect the expression of CYCD3;1 and the immune receptor gene SUPRESSOR OF npr1-1, CONSTITUTIVE (SNC)1. Additionally, CYCD3;1 overexpression enhances immune responses and SNC1 protein levels. Moreover, G1-S phase checkpoint proteins Rb and E2F engaged in immune-related PCD.

Taken together, these findings indicate that plants balance cell cycle regulation and immune response through manipulating the level of cyclins or the activation of CDKs. Plants respond to pathogen attack via arrested cell cycle progression depend on the state at which plants are attacked. At mitosis, inhibition of APC/C activation will contribute to immunity. At G1, S, or G2 phase, operating the expression of cyclins or check point proteins, such as E2Fs and MYB3R, are of good benefit to immunity. It’s reasonable to speculate that the biological significance of using cell cycle components as regulators of immunity is to turn cells from endoreduplication, which favors pathogen infection, to cell cycle arrest or cell death, and therefore prevent pathogen infection spread. Though recent studies have broadened our knowledge of immunity-cell cycle trade-off, future efforts are needed to identify the immunity-growth pathway and the detailed molecular mechanisms. Single-cell RNA sequence technology, RNA-Seq approach and proteomic analysis will help to underscore molecular connections that ensure antagonistic regulation of growth and immunity in plants under natural or abiotic stress conditions.

Cell Cycle Regulation and Abiotic Stress Adaptation

Salinity, temperature, moisture, and light are abiotic factors that influence plant growth and crop yield, which is shown to be a consequence of cell proliferation and the cell expansion. A rapid response to changing conditions is critical for successful adaptation. Plants respond to different stresses through a variety of mechanisms. In the following sections, we highlight the role of protein kinases that regulate cell cycle progression in the response to abiotic stressors.

Salt Stress

In general, high salinity leads to ion toxicity, water deficit, and oxidative stress. Osmotic stress also reduces cell division rates and cell numbers in leaves, roots, or the shoot meristem. Calcium ion (Ca2+) responses, reactive oxygen species (ROS) burst and abscisic acid (ABA)-dependent protein kinases are involved in response to high salinity. However, recent evidence has begun to underline the cell cycle regulator’s importance in stress response, especially cyclins and CDKs. A. thaliana, a non–salt-tolerant plant, is widely used as a model to investigate the molecular mechanisms of salt tolerance. Two CDKs have been identified in A. thaliana: AtCDC2a regulates the G1/S and G2/M transitions, whereas AtCDC2b is mainly expressed in S and G2 phases in meristem tissues. Upon NaCl treatment, the transcription of AtCDC2a and CYCA2;1 was decreased in the vascular cylinder of the root, which correlated with reduced lateral root formation. In root tips, AtCDC2a, CYCA2;1, and CYCB1;1 were downregulated along with reduced root growth (S et al., 2004; ). demonstrated that, in Arabidopsis thaliana roots, mild salt stress leads to loss of CDK activity and reduced promoter activity of CYCB1;2. Severe salt stress transiently decreases the expression levels of the cyclins CYCA2;1 and CYCB;1. In addition, revealed that heat and cold treatments both induced a pronounced cell accumulation in G2/M transition and NaCl treatment results in an extensive inhibition in both S and G2/M phase by analyzing DNA content in maize (Zea MAYS l). Furthermore, the perturbed cell cycle progression is attributed to the dynamic histone acetylation change which participated in the control of CDKs and cyclins transcription. Thus, high salinity affects cell cycle regulation via control the cell cycle regulators. However, molecular players which perceive Na+ ions and confer salt stress to regulated cyclins and CDKs are still need to be unraveled.

Interestingly, there exists a group of salt-tolerant plants which grow in highly saline soil or water called halophyte. An example of a halophyte is Suaeda salsa, which produces dimorphic seeds on the same plant, brown seeds but not black seeds are able to germinate under conditions of high salinity owing to the presence of a seed coat. In this species, ion transport signaling contributes to salt tolerance through the action of various genes including HIGH-AFFINITY POTASSIUM TRANSPORTER (SsHKT)1, SODIUM/HYDROGEN EXCHANGER (SsNHX)1, and ASCORBATE PEROXIDASE (SsAPX). Besides, S. salsa treated with 200 mM NaCl generated healthier seeds with higher starch, soluble sugar, protein, and lipid contents than those treated with other concentrations of NaCl. Another salt-tolerant plant is Limonium bicolor, a recretohalophyte with salt glands and a bladder that enable the secretion of excess salt into the environment. Recent studies show that the rate of secretion is determined by K+ and Ca2+ concentration. In Thellungiella salsuginea, microRNAs and unsaturated fatty acids enhance resistance to high salinity. It’s meaningful to detect whether the genes or microRNAs or unsaturated fatty acids mentioned above help to sustain the normal expression of cyclins and the activities of CDKs to some extent.

In conclusion, halophytes have evolved functional adaptations, ensuring their survival in saline environment. Analysis the difference between halophytes and glycophytes in transcriptomics and proteomics contributes to discover genes which is responsible for salt tolerance. Moreover, although most crop plants are glycophytes and are unable to tolerate high levels of salt stress, the abilities of glycophytes to withstand salt stress differ. This natural variation can be utilized to identify genetic components underlying salinity tolerance in glycophytes. Furthermore, screening proteins interacting with cyclins or CDKs under normal or stressed conditions are conductive to find molecules which confer salt stress signal to manipulated cell cycle regulators. Crops can be genetically engineered to resist high salinity through the expression of salt-responsive genes from halophytes; this has been demonstrated by the generation of salt-tolerant varieties of tomato, wheat, soybean, tobacco, peanut, cotton, and A. thaliana.

Temperature Stress

Plants are continually exposed to changes in the ambient temperature. Both chilling and hot can negatively affect plant growth and development. Temperature stress triggers Ca2+ fluxes, kinase cascades, and accumulation of abscisic acid. These factors activate cell cycle checkpoints that delay entry into mitosis. In plants, more and more evidence has emerged to reveal the molecular mechanisms that regulate CDK functions in adapt to temperature stress. Under mild heat stress, proliferating cells are transiently arrested at G1/S or G2/M phase in BY2 cells, depending on the stage at which the stress was applied. The arrested cell cycle partially due to the reduced transcription of CYCA and CYCB and, as a consequence, decreased CDK activity. On the other hand, high temperatures induce a signaling cascade that leads to programmed cell death.

demonstrated that the increased cell cycle time in meristem of leaves exposed to chilling was associated with the up-regulated expression of cell cycle inhibitors such as KPRS. Similarly, the EL2 gene from rice (Orysa;E2L) was induced to transcript by low temperature. Orysa;E2L is a plant specific inhibitor of CDK that inhibit CDKA1 activation during G1/S transition through direct or indirect binding to CYCD. In addition, cold stress stimulates the expression of the transcription factor OsMYB3R2, which increases the expression of several G2/M-specific genes such as OsCYCB1. Furthermore, OsCYCB1 overexpression increased resistance to cold stress. Moreover, many other cold-responsive genes have been identified in T. salsuginea and rice by RNA-sequencing. The T. salsuginea gene FILAMENTOUS TEMPERATURE-SENSITIVE H8 was shown to alleviate cold-induced photoinhibition. In rice (Oryza sativa), LOW-TEMPERATURE RESPONSE PROTEIN KINASE 1 contributes to cold resistance by regulating cytoskeletal rearrangement. Meanwhile, phytochrome B diminishes cold tolerance by modulating the expression of DEHYDRATION-RESPONSIVE ELEMENT-BINDING 1 and unsaturated fatty acid content (;;; He et al., 2016). Ectopic expression of the above genes increases the ability of crops to resist cold temperatures, although the underlying mechanisms are unclear. It’s of interest to investigate whether the different stress responsive genes work in the same signal pathway.

Put together, plants adjust to high-temperature and low-temperature via regulating the expression of different cell cycle machinery components. The fact that plants have larger number of cyclins compared with other eukaryotes may indicate cyclins function in stress response or perception to some degree. Most studies have revealed that temperature halt cell cycle progression through decrease or increase the transcript levels of related genes, however, we should take posttranslational modification of CDKs into consideration. Despite all of this, additional studies are needed to clarify the molecular basis for cell cycle regulators in response to hot or cold conditions.

Drought Stress

Drought stress is one of the abiotic stresses that limit plant growth and crop yield. Drought induces physiological changes in plants that enable survival, such as stomatal closure, perturbation of cell growth, and inhibition of photosynthesis. These processes involve the activation or repression of transcription factors, protein kinases, and metabolism-related enzymes. Here, we focus on the effect of drought on cell cycle proliferation and cell expansion. The growth of an organ is roughly divided into two stages: the cell proliferation stage, in which the cell number increases; and the cell expansion stage, in which cells expand to their final size. In Arabidopsis and sunflowers, water deficit affects both cell division and cell expansion. The reduced cell number in sunflower leaves was owing to the arrested G1/S transition. Progression to S phase is mediated by the activity of cyclin-dependent kinase A (CDKA). We can speculate that drought damages CDKA activity more or less. In wheat seedlings subjected to mild water stress, leaf elongation rate and mitotic activity were reduced in mesophyll cells due to decreased activity of CDKA1, which is required for entry into mitosis. This was accompanied by downregulation of cyclins and the accumulation of cells in G1 or G2 phase. Similarly, in maize leaves, cell division and CDKA1 activity was decreased in response to a mild water deficit, resulting in the inhibition of endosperm development. However, the amount of CDKA1 protein remained unaffected suggesting that posttranslational regulation of CDKA1 was responsible. In another drought-tolerant Brachypodium leaves, cell expansion is affected while cell proliferation is not, which is opposite to Arabidopsis and maize. The molecules response to drought stress strongly dependent on the developmental stage. In the leaf’s proliferation zone, drought stress had no effect on the expression of genes related to cell division. By Affymetrix tiling array analysis, the researchers identified numerous drought-responsive genes which were mainly expressed in the mature leaf zone. In summary, our current understanding of stress-regulated growth is still very fragmentary, partly because studies combining detailed growth analysis and molecular characterization of growing tissues are relatively scarce. Molecular characterization of the stress responses of growing tissues has to be investigated by further step. Broadening our knowledge of the mechanisms underlying growth reduction under stress is an important prerequisite to further improve crop productivity.

Conclusion and Perspectives

As sessile organisms, plants are frequently challenged as their environment changes during their lifetime. The ability of plants to perceive and adapt to these changes facilitates survival and production. Similarly, both biotic stress and abiotic stress perturb cell cycle progression and, at worst, lead to programmed cell death. Plants have evolved multiple mechanisms to defense against stresses. In brief, perception of biotic and abiotic stress signals activates signaling cascades that trigger ion fluxes, kinase cascades, reactive oxygen species production, and accumulation of hormones, such as abscisic acid (ABA) and jasmonic acid (JA). Theses signaling molecules suppress the activities of CDKs via controlling the expression level of cyclins or regulating the posttranslational modification of CDKs and, as a consequence, arrest the cell cycle or even exit cell cycle. This review highlights the role of cell cycle modulation in the adaption of plants to biotic and abiotic stresses and discusses the associated mechanisms proposed by recent studies ( Figure 2 ). Even though the existing studies indicate that CDKs and cyclins are important for the detection and adaptation to stress by plants, there still exist many outstanding questions regarding the relationship between plant defense responses and cell cycle kinetics. For instance, it is unclear whether cyclins are directly involved in sensing stresses and whether the cyclin molecules differ in sensing abiotic stress and biotic stress. Additionally, plant proteins that detect stress and transmit signals to delay cell cycle progression remain to be identified. Moreover, it’s unknown why elevating the transcription level of cyclins or manipulating CDK activities could, to some extent, increase the ability of plants to defense against stresses. Single cell RNA sequencing approach, high-throughput, genome-wide transcriptome and proteomic technologies will help us to identify new genes and proteins involved in stress response and then broad our knowledge about cell cycle regulation and response adaption. Fully understanding the molecular signal network which regulate stress response and cell growth is the prerequisite for researchers to elevate crop plants’ resistance to stresses and improve crop plants yield.

Author Contributions

FQ and FZ wrote the manuscript and FQ critically revised the manuscript. All authors approved the final version of the manuscript.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict interest.

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  34. 34.

    He C. Q. Liu Y. X. Wang H. M. Hou P. L. He H. B. Ding N. Z. (2016 ). New genetic mechanism, origin and population dynamic of bovine ephemeral fever virus. Vet. Microbiol. 182, 50–56.

    Not in our library10.1016/j.vetmic.2015.10.029

  35. 35.

    He Y. A. Li Y. P. Cui L. X. Xie L. X. Zheng C. K. Zhou G. H. (2016 ). Phytochrome B negatively affects cold tolerance by regulating OsDREB1 gene expression through phytochrome interacting factor-like protein OsPIL16 in Rice. Front. Plant Sci. 7 (1963).

    Not in our library10.3389/fpls.2016.01963

  36. 36.

    Hou L. Chen L. J. Wang J. Y. Xu D. F. Dai L. X. Zhang H. (2012 ). Construction of Stress responsive synthetic promoters and analysis of their activity in transgenic Arabidopsis thaliana. Plant Mol. Biol. Rep. 30 (6), 1496–1506.

    Not in our library10.1007/s00425-014-2135-x

  37. 37.

    Hou L. Liu W. Li Z. Huang C. Fang X. L. Wang Q. (2014 ). Identification and expression analysis of genes responsive to drought stress in peanut. Russ. J. Plant Physiol. 61 (6), 842–852.

    Not in our library10.1134/s1021443714060089

  38. 38.

    Hou P. L. Wang H. M. Zhao G. M. He C. Q. He H. B. (2017 ). Rapid detection of infectious bovine Rhinotracheitis virus using recombinase polymerase amplification assays. Bmc Vet. Res. 13 (1), 386.

    Not in our library10.1186/s12917-017-1284-0

  39. 39.

    Hou P. L. Zhao G. M. He C. Q. Wang H. M. He H. B. (2018 ). Biopanning of polypeptides binding to bovine ephemeral fever virus G(1) protein from phage display peptide library. Bmc Vet. Res. 14 (1), 3.

    Not in our library10.1186/s12917-017-1315-x

  40. 40.

    Huang Y. H. Wang X. J. Zhang F. Huo X. B. Fu R. S. Liu J. J. (2013 ). The Identification of a Bacterial strain BGI-1 Isolated From the Intestinal Flora of Blattella Germanica, and Its Anti-Entomopathogenic Fungi Activity. J. Econ. Entomol, 106 (1), 43–49.

    Not in our library10.1603/ec12120

  41. 41.

    Jang S. J. Shin S. H. Yee S. T. Hwang B. Im K. H. Park K. Y. (2005 ). Effects of abiotic stresses on cell cycle progression in Tobaco BY-2 Cells. Mol. Cells 20 (1), 136–141.

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  42. 42.

    Kadota Y. Watanabe T. Fujii S. Higashi K. Sano T. Nagata T. (2004 ). Crosstalk between elicitor-induced cell death and cell cycle regulation in tobacco BY-2 cells. Plant J. 40 (1), 131–142.

    Not in our library10.1111/j.1365-313x.2004.02197.x

  43. 43.

    Kadota Y. Watanabe T. Fujii S. Maeda Y. Ohno R. Higashi K. (2005 ). Cell cycle dependence of elicitor-induced signal transduction in tobacco BY-2 cells. Plant Cell Physiol. 46 (1), 156–165.

    Not in our library10.1093/pcp/pci008

  44. 44.

    Kim S. H. Son G. H. Bhattacharjee S. Kim H. J. Nam J. C. Nguyen P. D. (2014 ). The Arabidopsis immune adaptor SRFR1 interacts with TCP transcription factors that redundantly contribute to effector-triggered immunity. Plant J. 78 (6), 978–989.

    Not in our library10.1111/tpj.12527

  45. 45.

    Kong X. Q. Gao X. H. Sun W. An J. Zhao Y. X. Zhang H. (2011 ). Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1. Plant Mol. Biol. 75 (43363), 567–578.

    Not in our library10.1007/s11103-011-9744-6

  46. 46.

    Kong L. A. Xie Y. Hu L. Si J. S. Wang Z. S. (2017 ). Excessive nitrogen application dampens antioxidant capacity and grain filling in wheat as revealed by metabolic and physiological analyses. Sci. Rep. 7 (743363).

    Not in our library10.1038/srep43363

  47. 47.

    Larkindale J. Knight M. R. (2002 ). Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128 (2), 682–695.

    Not in our library10.1104/pp.128.2.682

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    Leng B. Y. Yuan F. Dong X. X. Wang J. Wang B. S. (2018 ). Distribution pattern and salt excretion rate of salt glands in two recretohalophyte species of Limonium (Plumbaginaceae). South Afr. J. Bot. 115, 74–80.

    Not in our library10.1016/j.sajb.2018.01.002

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    Li K. Pang C. H. Ding F. Sui N. Feng Z. T. Wang B. S. (2012 ). Overexpression of Suaeda salsa stroma ascorbate peroxidase in Arabidopsis chloroplasts enhances salt tolerance of plants. South Afr. J. Bot. 78, 235–245.

    Not in our library10.1016/j.sajb.2011.09.006

  50. 50.

    Li X. Liu Y. Chen M. Song Y. P. Song J. Wang B. S. (2012 ). Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations. Plant Biosyst. 146, 142–149.

    Not in our library10.1080/11263504.2012.727880

  51. 51.

    Li Z. Y. Li B. Dong A. W. (2012 ). The Arabidopsis transcription factor AtTCP15 regulates endoreduplication by modulating expression of key cell-cycle genes. Mol. Plant 5 (1), 270–280.

    Not in our library10.1093/mp/ssr086

  52. 52.

    Li H. Zhang F. M. Guo H. Y. Zhu Y. Y. Yuan J. D. Yang G. W. (2013 ). Molecular characterization of hepcidin gene in common carp (Cyprinus carpio L.) and its expression pattern responding to bacterial challenge. Fish Shellfish Immunol. 35 (3), 1030–1038.

    Not in our library10.1016/j.fsi.2013.07.001

  53. 53.

    Li H. Yang G. W. Ma F. Li T. Yang H. T. Rombout J. (2017 ). Molecular characterization of a fish-specific toll-like receptor 22 (TLR22) gene from common carp (Cyprinus carpio L.): Evolutionary relationship and induced expression upon immune stimulants. Fish Shellfish Immunol. 63, 74–86.

    Not in our library10.1016/j.fsi.2017.02.009

  54. 54.

    Li T. Li H. Peng S. Q. Zhang F. M. An L. G. Yang G. W. (2017 ). Molecular characterization and expression pattern of X box-binding protein-1 (XBP1) in common carp (Cyprinus carpio L.): Indications for a role of XBP1 in antibacterial and antiviral immunity. Fish Shellfish Immunol. 67, 667–674.

    Not in our library10.1016/j.fsi.2017.06.055

  55. 55.

    Liang J. W. Tian F. L. Lan Z. R. Huang B. Zhuang W. Z. (2010 ). Selection characterization on overlapping reading frame of multiple-protein-encoding P gene in Newcastle disease virus. Vet. Microbiol. 144 (3-4), 257–263.

    Not in our library10.1016/j.vetmic.2009.12.029

  56. 56.

    Liu X. Y. Ju Z. H. Wang L. L. Zhang Y. Huang J. M. Li Q. L. (2011 ). Six novel single-nucleotide polymorphisms in SPAG11 gene and their association with sperm quality traits in Chinese Holstein bulls. Anim. Reprod. Sci. 129 (1-2), 14–21.

    Not in our library10.1016/j.anireprosci.2011.10.003

  57. 57.

    Liu D. S. Hu J. F. Horvath D. P. Zhang X. J. Bian X. Y. Chang G. L. (2012 ). Invasions and Impacts of Alligatorweed in the Upper Xiaoqing River Basin of Northern China. J. Aquat. Plant Manag. 50, 19–24.

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  58. 58.

    Liu W. Ji S. X. Fang X. L. Wang Q. G. Li Z. Yao F. Y. (2013 ). Protein Kinase LTRPK1 Influences cold adaptation and microtubule stability in rice. J. Plant Growth Regul. 32 (3), 483–490.

    Not in our library10.1007/s00344-012-9314-4

  59. 59.

    Liu X. X. Fu C. Yang W. W. Zhang Q. Fan H. Liu J. (2016 ). The involvement of TsFtsH8 in Thellungiella salsuginea tolerance to cold and high light stresses. Acta Physiol. Plant. 38 (3).

    Not in our library10.1007/s11738-016-2080-3

  60. 60.

    Liu S. S. Wang W. Q. Li M. Wan S. B. Sui N. (2017 ). Antioxidants and unsaturated fatty acids are involved in salt tolerance in peanut. Acta Physiol. Plant. 39 (9). 207

    Not in our library10.1007/s11738-017-2501-y

  61. 61.

    Liu T. T. Liu S. Ma L. Li F. L. Zheng Z. D. Chai R. F. (2017 ). Oogenesis, vitellogenin-mediated ovarian degeneration and immune response in the annual fish Nothobranchius guentheri. Fish Shellfish Immunol. 66, 86–92.

    Not in our library10.1016/j.fsi.2017.05.015

  62. 62.

    Liu Q. Q. Liu R. R. Ma Y. C. Song J. (2018 ). Physiological and molecular evidence for Na+ and Cl- exclusion in the roots of two Suaeda salsa populations. Aquat. Bot. 146, 1–7.

    Not in our library10.1016/j.aquabot.2018.01.001

  63. 63.

    Ma Q. Dai X. Xu Y. Guo J. Liu Y. Chen N. (2009 ). Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol. 150 (1), 244–256.

    Not in our library10.1104/pp.108.133454

  64. 64.

    Meng X. Yang D. Y. Li X. D. Zhao S. Y. Sui N. Meng Q. W. (2015 ). Physiological changes in fruit ripening caused by overexpression of tomato SlAN2, an R2R3-MYB factor. Plant Physiol. Biochemi. 89, 24–30.

    Not in our library10.1016/j.plaphy.2015.02.005

  65. 65.

    Peres A. Churchman M. L. Hariharan S. Himanen K. Verkest A. Vandepoele K. (2007 ). Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J. Biol. Chem. 282 (35), 25588–25596.

    Not in our library10.1074/jbc.m703326200

  66. 66.

    Petutschnig E. K. Jones A. M. E. Serazetdinova L. Lipka U. Lipka V. (2010 ). The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 285 (37), 28902–28911.

    Not in our library10.1074/jbc.m110.116657

  67. 67.

    Qi Y. C. Liu W. Q. Qiu L. Y. Zhang S. M. Ma L. Zhang H. (2010 ). Overexpression of glutathione S-transferase gene increases salt tolerance of arabidopsis. Russ. J. Plant Physiol. 57 (2), 233–240.

    Not in our library10.1134/s102144371002010x

  68. 68.

    Rymen B. Fiorani F. Kartal F. Vandepoele K. Inzé D. Beemster G. T. (2007 ). Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol. 143 (3), 1429–1438.

    Not in our library10.1104/pp.106.093948

  69. 69.

    Schuppler U. He. P. H. John. P. C. Munns. R. (1998 ). Effect of water stress on cell division and Cdc2-Like cell cycle Kinase activity in wheat leaves. Plant Physiol. 117 (2), 667–678.

    Not in our library10.1104/pp.117.2.667

  70. 70.

    Shan S. J. Qi C. C. Zhu Y. Y. Li H. An L. G. Yang G. W. (2016 ). Expression profile of carp IFN correlate with the up-regulation of interferon regulatory factor-1 (IRF-1) in vivo and in vitro: the pivotal molecules in antiviral defense. Fish Shellfish Immunol. 52, 94–102.

    Not in our library10.1016/j.fsi.2016.03.019

  71. 71.

    Shan S. J. Liu D. Z. Liu R. R. Zhu Y. Y. Li T. Zhang F. M. (2018 ). Non-mammalian Toll-like receptor 18 (Tlr18) recognizes bacterial pathogens in common carp (Cyprinus carpio L.): Indications for a role of participation in the NF-kappa B signaling pathway. Fish Shellfish Immunol. 72, 187–198.

    Not in our library10.1016/j.fsi.2017.09.081

  72. 72.

    Shao Q. Han N. Ding T. L. Zhou F. Wang B. S. (2014 ). SsHKT1;1 is a potassium transporter of the C-3 halophyte Suaeda salsa that is involved in salt tolerance. Funct. Plant Biol. 41 (8), 790–802.

    Not in our library10.1071/fp13265

  73. 73.

    Shen X. Y. Wang Z. L. Song X. F. Xu J. J. Jiang C. Y. Zhao Y. X. (2014 ). Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis. Plant Mol. Biol. 86 (3), 303–317.

    Not in our library10.1007/s11103-014-0230-9

  74. 74.

    Song J. Wang B. S. (2015 ). Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann. Bot. 115 (3), 541–553.

    Not in our library10.1093/aob/mcu194

  75. 75.

    Song J. Shi G. W. Gao B. Fan H. Wang B. S. (2011 ). Waterlogging and salinity effects on two Suaeda salsa populations. Physiol. Plant. 141 (4), 343–351.

    Not in our library10.1111/j.1399-3054.2011.01445.x

  76. 76.

    Song J. Zhou J. C. Zhao W. W. Xu H. L. Wang F. X. Xu Y. G. (2016 ). Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Species Biol. 31 (1), 19–28.

    Not in our library10.1111/1442-1984.12071

  77. 77.

    Song J. Shi W. W. Liu R. R. Xu Y. G. Sui N. Zhou J. C. (2017 ). The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Species Biol. 32 (2), 107–114.

    Not in our library10.1111/1442-1984.12132

  78. 78.

    Sui N. Han G. L. (2014 ). Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids. Acta Physiol. Plant. 36 (4), 983–992.

    Not in our library10.1007/s11738-013-1477-5

  79. 79.

    Sui N. Li M. Li K. Song J. Wang B. S. (2010 ). Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity. Photosynthetica 48 (4), 623–629.

    Not in our library10.1007/s11099-010-0080-x

  80. 80.

    Sui N. Tian S. S. Wang W. Q. Wang M. J. Fan H. (2017 ). Overexpression of Glycerol-3-Phosphate Acyltransferase from Suaeda salsa Improves Salt Tolerance in Arabidopsis. Front. Plant Sci. 8 (1337).

    Not in our library10.3389/fpls.2017.01337

  81. 81.

    Sui N. (2015 ). Photoinhibition of Suaeda salsa to chilling stress is related to energy dissipation and water-water cycle. Photosynthetica 53 (2), 207–212.

    Not in our library10.1007/s11099-015-0080-y

  82. 82.

    Sun Y. L. Li F. Su N. Sun X. L. Zhao S. J. Meng Q. W. (2010 ). The increase in unsaturation of fatty acids of phosphatidylglycerol in thylakoid membrane enhanced salt tolerance in tomato. Photosynthetica 48 (3), 400–408.

    Not in our library10.1007/s11099-010-0052-1

  83. 83.

    Sun G. J. Pan J. Liu K. C. Wang S. F. Wang X. Wang X. M. (2012 ). Molecular cloning and expression analysis of P-selectin glycoprotein ligand-1 from zebrafish (Danio rerio). Fish Physiol. Biochemi. 38 (2), 555–564.

    Not in our library10.1007/s10695-011-9535-7

  84. 84.

    Sun Z. B. Qi X. Y. Wang Z. L. Li P. H. Wu C. X. Zhang H. (2013 ). Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol. Biochemi. 69, 82–89.

    Not in our library10.1016/j.plaphy.2013.04.009

  85. 85.

    Sun W. Li Y. Zhao Y. X. Zhang H. (2015 ). The TsnsLTP4, a nonspecific lipid transfer protein involved in wax deposition and stress tolerance. Plant Mol. Biol. Rep. 33 (4), 962–974.

    Not in our library10.1007/s11105-014-0798-x

  86. 86.

    Tang G. Y. Wei L. Q. Liu Z. J. Bi Y. P. Shan L. (2012 ). Ectopic expression of peanut acyl carrier protein in tobacco alters fatty acid composition in the leaf and resistance to cold stress. Biologia Plant. 56 (3), 493–501.

    Not in our library10.1007/s10535-012-0057-7

  87. 87.

    Tang G. Y. Shao F. X. Xu P. L. Shan L. Liu Z. J. (2017 ). Overexpression of a peanut NAC gene, AhNAC4, confers enhanced drought tolerance in tobacco. Russ. J. Plant Physiol. 64 (4), 525–535.

    Not in our library10.1134/s1021443717040161

  88. 88.

    Tian W. Zhang H. Y. Zhang J. Zhao L. Miao M. S. Huang H. (2017 ). Responses of Zooplankton community to environmental factors and phytoplankton biomass in lake Nansihu, China. Pak. J. Zool. 49 (2), 493–504.

    Not in our library10.17582/journal.pjz/2017.49.2.461.470

  89. 89.

    TL S. BA F. (2001 ). Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. J. Exp. Bot. 52 (360), 1401–1408.

    Not in our library10.1093/jexbot/52.360.1401

  90. 90.

    Vacca R. A. de Pinto M. C. Valenti D. Passarella S. Marra E. De Gara L. (2004 ). Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol. 134 (3), 1100–1112.

    Not in our library10.1104/pp.103.035956

  91. 91.

    Verbon E. H. Post J. A. Boonstra J. (2012 ). The influence of reactive oxygen species on cell cycle progression in mammalian cells. Gene 511 (1), 1–6.

    Not in our library10.1016/j.gene.2012.08.038

  92. 92.

    Wang S. S. Wang F. Tan S. J. Wang M. X. Sui N. Zhang X. S. (2014 ). Transcript profiles of maize embryo sacs and preliminary identification of genes involved in the embryo sac-pollen tube interaction. Front. Plant Sci. 5 (702).

    Not in our library10.3389/fpls.2014.00702

  93. 93.

    Wang X. G. Huang J. M. Feng M. Y. Ju Z. H. Wang C. F. Yang G. W. (2014 ). Regulatory mutations in the A2M gene are involved in the mastitis susceptibility in dairy cows. Anim. Genet. 45 (1), 28–37.

    Not in our library10.1111/age.12099

  94. 94.

    Wang F. X. Xu Y. G. Wang S. Shi W. W. Liu R. R. Feng G. (2015 ). Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiol. Biochemi. 95, 41–48.

    Not in our library10.1016/j.plaphy.2015.07.005

  95. 95.

    Wang F. R. Zhang C. Y. Liu G. D. Chen Y. Zhang J. X. Qiao Q. H. (2016 ). Phenotypic variation analysis and QTL mapping for cotton (Gossypium hirsutum L.) fiber quality grown in different cotton-producing regions. Euphytica 211 (2), 169–183.

    Not in our library10.1007/s10681-016-1728-9

  96. 96.

    Wang J. S. Zhang Q. Cui F. Hou L. Zhao S. Z. Xia H. (2017 ). Genome-Wide analysis of gene expression provides new insights into cold responses in Thellungiella salsuginea. Front. Plant Sci. 8 (713).

    Not in our library10.3389/fpls.2017.00713

  97. 97.

    Weng L. Tian Z. X. Feng X. Z. Li X. Xu S. L. Hu X. H. (2011 ). Petal development in Lotus japonicus. J. Integr. Plant Biol. 53 (10), 770–782.

    Not in our library10.1111/j.1744-7909.2011.01072.x

  98. 98.

    West G. Inze D. Beemster G. T. (2004 ). Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol. 135 (2), 1050–1058.

    Not in our library10.1104/pp.104.040022

  99. 99.

    Xing N. Ji L. Z. Song J. Ma J. C. Li S. G. Ren Z. M. (2017 ). Cadmium stress assessment based on the electrocardiogram characteristics of zebra fish (Danio rerio): QRS complex could play an important role. Aquat. Toxicol. 191, 236–244.

    Not in our library10.1016/j.aquatox.2017.08.015

  100. 100.

    Xu Y. G. Liu R. R. Sui N. Shi W. W. Wang L. Tian C. Y. (2016 ). Changes in endogenous hormones and seed-coat phenolics during seed storage of two Suaeda salsa populations. Aust. J. Bot. 64 (4), 325–332.

    Not in our library10.1071/bt16014

  101. 101.

    Yang M. F. Song J. Wang B. S. (2010 ). Organ-Specific responses of vacuolar H+-ATPase in the shoots and roots of C-3 Halophyte Suaeda salsa to NaCl. J. Integr. Plant Biol. 52 (3), 308–314. CNKISUNZWXB.0.2010-03-007

    Not in our library10.1111/j.1744-7909.2010.00895.x

  102. 102.

    Yang J. C. Li M. Xie X. Z. Han G. L. Sui N. Wang B. S. (2013 ). Deficiency of Phytochrome B alleviates chilling-induced photoinhibition in rice. Am. J. Bot. 100 (9), 1860–1870.

    Not in our library10.3732/ajb.1200574

  103. 103.

    Yang H. T. Zou S. S. Zhai L. J. Wang Y. Zhang F. M. An L. G. (2017 ). Pathogen invasion changes the intestinal microbiota composition and induces innate immune responses in the zebrafish intestine. Fish Shellfish Immunol. 71, 35–42.

    Not in our library10.1016/j.fsi.2017.09.075

  104. 104.

    Yang Z. Wang Y. Wei X. C. Zhao X. Wang B. S. Sui N. (2017 ). Transcription Profiles of genes related to hormonal regulations under salt stress in sweet Sorghum. Plant Mol. Biol. Rep. 35 (6), 586–599.

    Not in our library10.1007/s11105-017-1047-x

  105. 105.

    Yoshida H. Lareau C. A. Ramirez R. N. Rose S. A. Maier B. Wroblewska A. (2019 ). The cis-Regulatory Atlas of the mouse immune system. Cell 176 (4), 897–912 e820.

    Not in our library10.1016/j.cell.2018.12.036

  106. 106.

    Yu J. Wu J. Q. Zhang Y. Y. Guo L. H. Cong X. Y. Du Y. J. (2012 ). Concurrent highly pathogenic porcine reproductive and respiratory syndrome virus infection accelerates Haemophilus parasuis infection in conventional pigs. Vet. Microbiol. 158 (3-4), 316–321.

    Not in our library10.1016/j.vetmic.2012.03.001

  107. 107.

    Yuan F. Chen M. Leng B. Y. Wang B. S. (2013 ). An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion. South Afr. J. Bot. 88, 110–117.

    Not in our library10.1016/j.sajb.2013.06.007

  108. 108.

    Yuan F. Chen M. Yang J. C. Leng B. Y. Wang B. S. (2014 ). A system for the transformation and regeneration of the recretohalophyte Limonium bicolor. Vitro Cell. Dev. Biology-Plant 50 (5), 610–617.

    Not in our library10.1007/s11627-014-9611-7

  109. 109.

    Yuan F. Chen M. Yang J. C. Song J. Wang B. S. (2015 a). The optimal dosage of Co-60 gamma irradiation for obtaining salt gland mutants of exo-recreyohalophyte limonium bicolor (Bunge) O. Kuntze. Pak. J. Bot. 47 (1), 71–76.

    Not in our library

  110. 110.

    Yuan F. Lyu M. J. A. Leng B. Y. Zheng G. Y. Feng Z. T. Li P. H. (2015 b). Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation. Plant Cell Environ. 38 (8), 1637–1657.

    Not in our library10.1111/pce.12514

  111. 111.
    Progress in Studying Salt Secretion from the Salt Glands in Recretohalophytes: How Do Plants Secrete Salt? · 2016
    No notice
  112. 112.

    Yuan F. Lyu M. J. A. Leng B. Y. Zhu X. G. Wang B. S. (2016 b). The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland. Plant Mol. Biol. 91 (3), 241–256.

    Not in our library10.1007/s11103-016-0460-0

  113. 113.

    Zebell S. G. Dong X. (2015 ). Cell-Cycle Regulators and Cell Death in Immunity. Cell Host Microbe 18 (4), 402–407.

    Not in our library10.1016/j.chom.2015.10.001

  114. 114.

    Zhang S. R. Song J. Wang H. Feng G. (2010 ). Effect of salinity on seed germination, ion content and photosynthesis of cotyledons in halophytes or xerophyte growing in Central Asia. J. Plant Ecol. 3 (4), 259–267.

    Not in our library10.1093/jpe/rtq005

  115. 115.

    Zhang Q. Zhao C. Z. Li M. Sun W. Liu Y. Xia H. (2013 ). Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response. Bmc Plant Biol. 13.

    Not in our library10.1186/1471-2229-13-180

  116. 116.

    Zhang F. Wang X. J. Huang Y. H. Zhao Z. G. Zhang S. S. Gong X. S. (2014 ). Differential expression of hemolymph proteins between susceptible and insecticide-resistant Blattella germanica (Blattodea: Blattellidae). Environ. Entomol, 43 (4), 1117–1123.

    Not in our library10.1603/en13351

  117. 117.

    Zhang F. M. Liu D. Z. Wang L. Li T. Chang Q. An L. G. (2015 ). Characterization of IgM-binding protein: A pIgR-like molecule expressed by intestinal epithelial cells in the common carp (Cyprinus carpio L.). Vet. Immunol. Immunopathol. 167 (1-2), 30–35.

    Not in our library10.1016/j.vetimm.2015.06.015

  118. 118.

    Zhang T. Song J. Fan J. L. Feng G. (2015 ). Effects of saline-waterlogging and dryness/moist alternations on seed germination of halophyte and xerophyte. Plant Species Biol. 30 (3), 231–236.

    Not in our library10.1111/1442-1984.12056

  119. 119.

    Zhang L. Y. Zhang X. J. Fan S. J. (2017 ). Meta-analysis of salt-related gene expression profiles identifies common signatures of salt stress responses in Arabidopsis. Plant Syst. Evol. 303 (6), 757–774.

    Not in our library10.1007/s00606-017-1407-x

  120. 120.

    Zhang Y. J. Kong X. Q. Dai J. L. Luo Z. Li Z. H. Lu H. Q. (2017 ). Global gene expression in cotton (Gossypium hirsutum L.) leaves to waterlogging stress. Plos One 12 (9). e0185075.

    Not in our library10.1371/journal.pone.0185075

  121. 121.

    Zhang N. Wang Z. Bao Z. Yang L. Wu D. Shu X. (2018 ). MOS1 functions closely with TCP transcription factors to modulate immunity and cell cycle in Arabidopsis. Plant J. 93 (1), 66–78.

    Not in our library10.1111/tpj.13757

  122. 122.

    Zhao K. F. Song J. Fan H. Zhou S. Zhao M. (2010 ). Growth response to ionic and osmotic stress of NaCl in Salt-tolerant and Salt-sensitive Maize. J. Integr. Plant Biol. 52 (5), 468–475.

    Not in our library10.1111/j.1744-7909.2010.00947.x

  123. 123.

    Zhao S. Z. Sun H. Z. Chen M. Wang B. S. (2010 ). Light-regulated betacyanin accumulation in euhalophyte Suaeda salsa calli. Plant Cell Tissue Organ Cult. 102 (1), 99–107.

    Not in our library10.1007/s11240-010-9710-z

  124. 124.

    Zhao S. Z. Sun H. Z. Gao Y. Sui N. Wang B. S. (2011 ). Growth regulator-induced betacyanin accumulation and dopa-4,5-dioxygenase (DODA) gene expression in euhalophyte Suaeda salsa calli. Vitro Cell. Dev. Biology-Plant 47 (3), 391–398.

    Not in our library10.1007/s11627-011-9339-6

  125. 125.

    Zhao L. Ding Q. Zeng J. Wang F. R. Zhang J. Fan S. J. (2012 ). An improved CTAB-Ammonium Acetate method for total RNA isolation from cotton. Phytochem. Anal. 23 (6), 647–650.

    Not in our library10.1002/pca.2368

  126. 126.

    Zhao L. Wang P. Hou H. Zhang H. Wang Y. Yan S. (2014 ). Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS One. 9 (8), e106070.

    Not in our library10.1371/journal.pone.0106070

  127. 127.

    Zhao X. Y. Zheng Z. W. Shang Z. Y. Wang J. Cheng R. Q. Qian J. L. (2014 ). Climatic information recorded in stable carbon isotopes in tree rings of Cryptomeria fortunei, Tianmu Mountain, China. Dendrochronologia 32 (3), 256–265.

    Not in our library10.1016/j.dendro.2014.06.002

  128. 128.

    Zhao B. T. Dai A. H. Wei H. C. Yang S. X. Wang B. S. Jiang N. (2016 ). Arabidopsis KLU homologue GmCYP78A72 regulates seed size in soybean. Plant Mol. Biol. 90 (1-2), 33–47.

    Not in our library10.1007/s11103-015-0392-0

  129. 129.

    Zhao S. S. Jiang Y. X. Zhao Y. Huang S. J. Yuan M. Zhao Y. X. (2016 ). CASEIN KINASE1-LIKE PROTEIN2 regulates actin filament stability and stomatal Closure via Phosphorylation of Actin Depolymerizing Factor. Plant Cell 28 (6), 1422–1439.

    Not in our library10.1105/tpc.16.00078

  130. 130.

    Zheng S. Wu X. Zhang L. Xin C. Liu Y. Shi J. (2017 ). The occurrence of porcine circovirus 3 without clinical infection signs in Shandong Province. Transbound. Emerg. Dis. 64 (5), 1337–1341.

    Not in our library10.1111/tbed.12667

  131. 131.

    Zheng Y. Liao C. C. Zhao S. S. Wang C. W. Guo Y. (2017 ). The Glycosyltransferase QUA1 regulates Chloroplast-Associated calcium signaling during salt and drought stress in Arabidopsis. Plant Cell Physiol. 58 (2), 329–341.

    Not in our library10.1093/pcp/pcw192

  132. 132.

    Zheng S. Shi J. Wu X. Peng Z. Xin C. Zhang L. (2018 ). Presence of Torque teno sus virus 1 and 2 in porcine circovirus 3-positive pigs. Transbound. Emerg. Dis. 65 (2), 327–330.

    Not in our library10.1111/tbed.12792

  133. 133.

    Zhou J. J. Liu Q. Q. Zhang F. Wang Y. Y. Zhang S. Y. Cheng H. M. (2014 ). Overexpression of OsPIL15, a phytochromeinteracting factor- like protein gene, represses etiolated seedling growth in rice. J. Integr. Plant Biol. 56 (4), 373–387.

    Not in our library10.1111/jipb.12137

  134. 134.

    Zhou J. C. Fu T. T. Sui N. Guo J. R. Feng G. Fan J. L. (2016 ). The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosyst. 150 (1), 83–90.

    Not in our library10.1080/11263504.2014.976294

  135. 135.

    Zhu Y. Y. Qi C. C. Shan S. J. Zhang F. M. Li H. An L. G. (2016 a). Characterization of common carp (Cyprinus carpio L.) interferon regulatory factor 5 (IRF5) and its expression in response to viral and bacterial challenges. Bmc Vet. Res. 12 (1), 127

    Not in our library10.1186/s12917-016-0750-4

  136. 136.

    Zhu Y. Y. Xing W. X. Shan S. J. Zhang S. Q. Li Y. Q. Li T. (2016 b). Characterization and immune response expression of the Rig-I-like receptor mda5 in common carp Cyprinus carpio. J. Fish Biol. 88 (6), 2188–2202.

    Not in our library10.1111/jfb.12981

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