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Review

Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways

by
Jaroslav Pavlů
1,2,†,
Jan Novák
1,†,
Vladěna Koukalová
1,
Markéta Luklová
1,2,
Břetislav Brzobohatý
1,2,3 and
Martin Černý
1,4,*
1
Department of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 613 00 Brno, Czech Republic
2
CEITEC—Central European Institute of Technology, Faculty of AgriSciences, Mendel University in Brno, 613 00 Brno, Czech Republic
3
Institute of Biophysics AS CR, 612 00 Brno, Czech Republic
4
Phytophthora Research Centre, Faculty of AgriSciences, Mendel University in Brno, 613 00 Brno, Czech Republic
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2018, 19(8), 2450; https://doi.org/10.3390/ijms19082450
Submission received: 27 July 2018 / Revised: 14 August 2018 / Accepted: 17 August 2018 / Published: 19 August 2018
(This article belongs to the Special Issue Phytohormones and Their Crosstalk during Plant Growth, Development and Environmental Stress Adaptation)
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Abstract

:
Cytokinin is a multifaceted plant hormone that plays major roles not only in diverse plant growth and development processes, but also stress responses. We summarize knowledge of the roles of its metabolism, transport, and signalling in responses to changes in levels of both macronutrients (nitrogen, phosphorus, potassium, sulphur) and micronutrients (boron, iron, silicon, selenium). We comment on cytokinin’s effects on plants’ xenobiotic resistance, and its interactions with light, temperature, drought, and salinity signals. Further, we have compiled a list of abiotic stress-related genes and demonstrate that their expression patterns overlap with those of cytokinin metabolism and signalling genes.

Graphical Abstract

1. Introduction

As sessile organisms, plants have evolved elaborate mechanisms that enable them to sense and respond to changes in environmental conditions, and are thus crucial for their adaptation and survival. These mechanisms involve abiotic stimuli triggering wide arrays of local and long-distance signals initiating developmental processes and stress responses that are regulated and coordinated by common integrative pathways. One of the key transmitted signals is cytokinin: a multifaceted plant hormone that plays major roles in diverse plant growth and development processes. Cytokinin signalling cascades are evolutionarily related to the two-component systems in unicellular organisms that participate in transduction of signals that are triggered by various environmental stimuli, for example, changes in temperature, nutrient levels, chemoattractants, or osmotic conditions [1,2,3]. In contrast to ethylene, another phytohormone that is involved in a two-component signalling pathway, cytokinin was not traditionally considered part of the primary stress response machinery. However, more recently, cytokinin crosstalk with ethylene and other so-called “stress hormones” (jasmonate, salicylic acid and abscisic acid) has been recognized (e.g., [4]), and current evidence indicates that it could be a primary perceptor in temperature or nutrient sensing. In the following text, we present an overview of cytokinin crosstalk with abiotic stimuli, as outlined in Figure 1. The presented evidence includes findings from compilation of a list of abiotic stress-related genes and analyses showing that their expression patterns overlap with those of cytokinin metabolism and signalling genes. Similarities in expression profiles mentioned here are expressed as percentages that are derived by multivariate analysis from average profiles.

2. Nutrient Stress

Plants require a number of elements for their growth and development. Besides carbon, hydrogen, and oxygen, which are primarily obtained from carbon dioxide and water, plants actively take up at least 20 elements. These include both macronutrients (nitrogen, phosphorus, sulphur, potassium), and micronutrients (including boron, iron, silicon and selenium). As discussed in the following text, cytokinin plays a pivotal role in plants’ uptake of these nutrients, and their responses to toxic metal(loid)s, including cadmium, aluminium, and arsenite.

2.1. Nitrogen

Nitrogen is one of the most strongly growth-limiting nutrients for plants. Thus, their internal nitrogen status and both the availability and distribution of nitrogen in their growth media are sensed by a complex network of signalling pathways that generate and regulate integrated responses to local and long-distance signals, including several phytohormones [6,7,8,9]. A well-known connection between nitrogen metabolism and cytokinin is nitrate supplementation-induced cytokinin biosynthesis in the roots. In Arabidopsis, the availability of nitrate regulates cytokinin biosynthesis rates by controlling the expression of the enzymes that catalyse the first rate-limiting step, isopentenyl transferase (IPT3, IPT5), and subsequent production of trans-Zeatin (tZ)-type cytokinins, cytochrome P450 (CYP735A2) [10,11]. In addition to these cytokinin metabolism genes, genes encoding cytokinin-responsive type-A response regulators (ARRs) and Cytokinin Response Factors (CRFs) are regulated by nitrate, but not ammonium, in Arabidopsis [12,13,14,15]. The signalling components that are involved in nitrate-upregulated cytokinin biosynthesis are the nitrate transporter-receptor NRT1 (NPF6.3) acting upstream of IPT3 [16], and the NLP-NIGT1 transcriptional cascade controlling CYP735A2 and IPT3 expression [17]. Cytokinin also participates in nitrate foraging, which involves plants’ preferential development of lateral roots in nitrate-rich areas, thereby maximizing nitrate acquisition [18,19,20]. The transcription factor TCP20, which controls the nitrate foraging response [9,21], can also bind to promoters of type-A ARR5/7, providing an additional link between nitrogen and cytokinin signalling [18,19]. Thus, the disruption of cytokinin signalling affects nitrate uptake, as demonstrated in the Arabidopsis cytokinin signalling mutant arr1,10,12. In this genotype, the nitrate-mediated induction of glutaredoxin genes (GRX) responsible for nitrate-mediated induction of primary root growth is abolished [22]. Moreover, RNA silencing of AtGRX3/4/5/7/8 has demonstrated that GRXs act downstream of cytokinin in a signal transduction pathway, which, in this case, suppresses plants’ primary root growth when nitrate supplies are sufficient [22,23]. Our meta-analysis (which included a comparison of expression patterns of all known cytokinin metabolism and signalling genes to those of 43 genes that respond to nitrogen deficiency) provided further evidence of cytokinin’s involvement in nitrate signalling. Expression patterns of seven and eight cytokinin signalling and metabolism genes, respectively, showed high similarity (>85%) to those of nitrogen deficiency genes. Overlaps were the strongest for the cytokinin biosynthetic gene APT2, which had a similar expression profile to five nitrogen-deficiency genes. For details, see Table 1 and Figure 2, Figure 3 and Figure 4.
In the shoot, root-derived cytokinins have been shown to mediate nitrate responses and modulate key traits, such as leaf size [24,25] and meristem activity-related traits [26]. Following its nitrate-induced synthesis in the root, cytokinin acts as a long-distance (systemic) signal, conveying information about the root’s nitrogen status that influences shoot metabolism and growth [12,27,28,29,30]. Cytokinin translocation via xylem in this systemic nitrogen response system is mediated by the cytokinin transporter ABCG14, and recent transcriptomic analysis indicates that its target could be the glutamate/glutamine metabolism machinery in the shoot [20,31]. Recent findings also show that long-distance transport of the cytokinin precursor tZR (which has low activity) can account for nitrate availability-mediated adjustments of shoot apical meristem size and organogenesis rates through modulating the expression of WUSCHEL [32]. Root-to-shoot cytokinin signalling operates in both directions, and, for example, lateral root growth is regulated by tZ content in the shoot [18,19,20].

2.2. Phosphorus

Like nitrogen sensing, a complex signalling system is required to maintain inorganic phosphate (Pi) homeostasis, and plants’ responses to Pi-limiting conditions involve multiple phytohormones [34,35]. As in nitrate sensing, one of the strongly affected cytokinin genes is the biosynthetic gene IPT3. Pi shortage causes the downregulation of IPT3 [36] and cytokinin signalling components, including the cytokinin receptor AHK4 [37]. Conversely, the resupply of Pi after a shortage causes upregulation of IPT3, CRF5, and CRF6 [38]. Moreover, reductions in root cytokinin levels upregulate the expression of Pi transporters [39,40,41,42] and the exogenous supply of cytokinin can suppress Pi uptake and Pi starvation responses in Arabidopsis and rice [37,43,44,45,46,47,48], presumably by mobilizing Pi from internal sources (preferentially stores in shoot tissues) [46]. This may temporarily reduce Pi starvation signalling and contribute to the relief of Pi deficiency symptoms, including the reported moderation of shoot growth inhibition of Pi-starved plants in the presence of cytokinin [49]. It has been proposed that the level of cell-cycle activity governs the magnitude of Pi demand in Pi-starved plants. This would fit well with cytokinin’s opposite effects on cell cycling in shoot and root meristems, where it, respectively, stimulates and represses cell division [50]. Further, auxin-cytokinin crosstalk via the auxin responsive factor OsARF16 regulates Pi signalling, and transport of Pi from roots to shoots [47].

2.3. Potassium

Potassium is the most abundant inorganic cation in plants, and it is one of the primary macronutrients that are generally added (together with nitrogen and phosphorus) to soil in fertilizers. Analysis of Arabidopsis plants has shown that potassium deprivation reduces cytokinin contents, and cytokinin signalling regulates root growth inhibition and potassium uptake [51]. The cited authors also found that cytokinin-deficient plants have enhanced the tolerance of potassium deficiency, which they attributed to the stimulation of ROS accumulation, root hair growth, and expression of HAK5, which encodes a potassium uptake transporter. This transporter connects multiple phytohormonal networks, as it is also regulated by ethylene [52] and participates in the modulation of the auxin transporter PIN1’s localization [53]. We found no significant similarity between expression patterns of HAK5 and any cytokinin metabolism/signalling genes. However, expression patterns of genes encoding seven potassium-deficiency-related genes (four potassium transporters, two antiporters, and a potassium channel) showed ≥85% similarity to those of candidate cytokinin genes (Table 1, Figure 2).

2.4. Sulphur

The availability of sulphur in soil is directly associated with crop yields and quality, and sulphur deficiency induces a number of adaptive responses [54]. A link between sulphur deficiency and responses in cytokinin status is indicated by IPT3 downregulation in roots of Arabidopsis plants grown on sulphur-deficient media [36], and observed changes in cytokinin contents triggered by sulphur deficiency in poplar [55]. In addition, exogenous application of cytokinin upregulates expression of sulphur-responsive genes in leaves [36]. By contrast, cytokinin downregulates the root expression of sulphate transporters (SULTR1;1 and SULTR1;2) that are involved in sulphate acquisition from the soil [39,56], and the arr1,10,12 triple mutant displays sulphur-deficiency-like gene expression patterns [57]. Thus, complex interplay between cytokinin and sulphur signalling, which is possibly mediated by independent regulatory circuits, is likely involved. The sulphur-deficiency marker gene GGCT2;1 encodes a key enzyme of glutathione degradation and it is a highly cytokinin-responsive gene [58], suggesting that cytokinin may participate in glutathione homeostasis and cytokinin-mediated glutathione decomposition may play a physiologically important role in nutrient mobilization.

2.5. Boron

Boron is an essential micronutrient for the growth of higher plants but there is a very narrow range between deficient and toxic concentrations [59]. Symptoms of severe boron deficiency include root growth inhibition, perturbances in root morphology, and reductions in vegetative and reproductive growth. Early detectable changes in boron-deficient plants include disturbances of hormonal metabolism and several lines of evidence suggest that ethylene and auxin are involved in the regulation of boron stress responses [60]. Boron deprivation induces the downregulation of cytokinin signalling genes [61,62], and our meta-analysis showed that BOR4, encoding a boron transporter, has a similar expression pattern to ARR1 and the cytokinin metabolism gene LOG7. Moreover, in oilseed rape, the shoot boron concentration reportedly correlates closely with cytokinin content, and boron enhances both cytokinin synthesis and the conversion of weakly active cytokinins to highly active forms [63]. Conversely, recent analysis indicates that boron deficiency inhibits root meristem growth via a molecular mechanism involving the cytokinin-mediated repression of cyclin CYCD3 [64].

2.6. Iron

Cytokinin suppresses expression of several genes that respond to iron deficiency in Arabidopsis [65]. This cytokinin-induced repression is mediated via AHK3 and AHK4 receptors, and it targets genes encoding components of the iron-uptake machinery (FRO2, IRT1) and the iron-deficiency induced transcription factor FIT1. The repression does not reflect the plant’s iron nutritional status, and analysis of a fit1 loss-of-function mutant indicates that it acts via a distinct, FIT1-independent signalling pathway [65]. This could be mediated by the ARF16 transcription factor, which is required for iron deficiency responses in rice [66] and participates in the auxin-cytokinin control of phosphate homeostasis [47]. Only five of 38 selected genes that are related to iron-deficiency had similar expression profiles to cytokinin regulatory genes. Moreover, the expression pattern of NRAMP4 (encoding a transporter of iron and several other metals) is similar to that of CKX (encoding a cytokinin degradation enzyme) and ARR1, but NRAMP4 expression is not reportedly upregulated by exogenous application of cytokinin [65]. Thus, this coregulation is unlikely to reflect iron status signalling.

2.7. Silicon

Silica minerals are major soil components, and high silicon uptake, boosted by root silicon transporters, promotes plants’ tolerance to many biotic and abiotic stresses. Mineralized (insoluble) silica provides structural support for many plants, but it can also enhance various defence mechanisms of plants and influence their stress responses by modulating their hormonal balance [67,68]. The beneficial effects of silicon are partially mediated by cytokinin [69]. Inter alia, silicic acid induces the cytokinin synthesis gene IPT7 and silicon accumulation delays dark-induced leaf senescence through the activation of cytokinin pathways in sorghum and Arabidopsis [70].

2.8. Selenium

At low concentrations, selenium promotes plant growth and stress resistance [71,72], but elevated levels can be toxic. Selenate and selenite, the two major forms of selenium that are found in the environment, are readily absorbed by plants via sulphate and phosphate transporters, respectively [73]. In this respect, cytokinin-regulated sulphate and Pi pathways might form a point of cross-talk between selenium and cytokinin signalling. For instance, the cytokinin-responsive sulphate transporter SULTR1;2 is a determinant of selenium tolerance in Arabidopsis [74]. Cytokinin signalling is promoted in the root tip of selenite-exposed Arabidopsis plants, and high cytokinin levels reportedly improve the performance of selenite-exposed roots, whereas reductions in cytokinin status or sensitivity enhance selenite sensitivity [75,76,77]. Recently, a selenium-tolerant Arabidopsis mutant with a loss-of-function mutation in a terpenoid synthase gene (TPS22) has been described. Observed effects of the mutation include reductions in cytokinin levels and the expression of cytokinin receptors AHK3 and AHK4, while the application of exogenous cytokinin upregulated selenocysteine methyltransferase (as well as high-affinity phosphate transporters) and decreased selenium tolerance of the mutant [42].

2.9. Xenobiotics

Strict control of processes that are involved in plants’ absorption, translocation, and storage of essential metals is crucial for the maintenance of their concentrations within physiological ranges and the avoidance of toxicity. Nevertheless, despite the transport systems’ selectivity, they may also take up toxic, non-essential metals and metalloids, such as arsenic, cadmium, chromium, lead, and mercury. Responses to these toxic xenobiotics, including cadmium [78] and aluminium [79], involve increases in cytokinin biosynthesis and signalling that inhibit root growth. Accordingly, application of substances that reduce active cytokinin contents or signalling can mitigate the adverse effects of cadmium [80]. Similarly, the cytokinin signalling component CRF6 is induced by organic xenobiotics, including the herbicide atrazine [81,82] and atrazine inhibition is weaker in the crf6 insertional mutant line than in wild-type plants [83]. Moreover, cytokinin-deficient plants grown in cadmium-contaminated soil reportedly accumulate more cadmium [39] and display enhanced arsenate tolerance [41], which is likely due to higher levels of thiol compounds [41]. Cytokinin also induces the upregulation of glutathione-S-transferase GSTU26 [84,85] and may thus play a role in glutathione conjugation.

3. Cytokinin Roles in Drought and Salinity Tolerance

Drought and salinity stress are the most frequent abiotic stresses and both impair crop production on a global scale [86]. Analysis of natural variants of Arabidopsis has shown that even mild drought can adversely affect plants if they are not evolutionarily adapted to it [87]. Plants react to water-limiting conditions by reducing their cytokinin levels, mainly through the modulation of cytokinin metabolism—as shown (inter alia) in Arabidopsis, creeping bentgrass, soybean, tobacco, and sunflower [88,89,90,91,92,93]—and/or the regulation of cytokinin receptors’ expression [94,95]. However, other mechanisms, including activation of the negative regulators of cytokinin signalling AHP6 and ARR5 also probably participate in this process [94,96,97]. Appropriate modulation of cytokinin metabolism and signalling has been known to improve drought and salt tolerance for many years [92,95,98,99], and at least five mechanisms may contribute to cytokinin-mediated enhancement of tolerance of water deficiency. These are: protection of the photosynthetic machinery, enhancement of antioxidant systems, improvement in water balance regulation, modulation of plant growth and differentiation, and modulation of activities of stress-related phytohormones.

3.1. Cytokinin Modulates Photosynthesis under Water-Limiting Conditions and Salt Stress

Changes in cytokinin status (mainly increases in cytokinin levels) reportedly enhance photosynthesis and related processes under water-deficiency or salt stress in many plant species [99,100,101,102,103,104], by increasing the expression of genes that are involved in photosynthesis, chlorophyll levels, photochemical efficiency, photochemical quenching, electron transport rates, and/or CO2 assimilation. Accordingly, in transgenic barley plants ectopically expressing the cytokinin-degradation enzyme AtCKX1, reductions in CO2 assimilation rates, accompanied by lower stomatal conductance, have been recorded [105]. Conversely, increases in CO2 assimilation have been observed in barley lines overexpressing CKX under a different promoter resulting in localization to different compartments. However, the cited authors only presented results from plants with elevated concentrations of tZ-type cytokinins [106]. It has been previously demonstrated that CKX overexpression stimulates cytokinin biosynthesis [107], so the observed positive effect on CO2 assimilation was likely due to increases in cytokinin content.

3.2. Cytokinin Enhances Capacities of Antioxidant Systems

Ectopic expression of ipt reportedly increases the capacities of plants’ antioxidant systems, including levels of antioxidants during severe drought stress [100]. This could protect their cells from excessive stress-induced ROS accumulation, thereby preserving chloroplast integrity [100,108,109] and reducing electrolyte leakage and/or rises in malondialdehyde levels [57,89,110]. On the other hand, ectopic expression of CKX in barley has been found to activate genes putatively involved in flavonoid biosynthesis [105] and flavonoids also participate in drought tolerance [111]. These effects of cytokinin in drought stress tolerance could involve indirect priming of antioxidant systems in response to manipulation of cytokinin homeostasis. In accordance with this hypothesis, significant enhancement of cytokinin biosynthesis can induce hypersensitivity-like responses and ROS-mediated cell death [112].

3.3. Cytokinin Influences Water Balance Regulation

Clearly, water management is crucial for drought tolerance, and plants with low levels of cytokinin or weak cytokinin signalling generally have higher water contents during drought stress than counterparts with higher cytokinin contents or stronger signalling [92,95,105]. This could be due to better root systems, since cytokinin is a known negative regulator of root growth and lateral root formation [106,110]. The improved water uptake in these plants is clearly complemented with reductions in transpiration rates and stomatal apertures, which could protect them from severe water losses during stress periods [57,105,110]. Ectopic expression of ipt also reduces water losses in plants that are exposed to drought, even when they have higher transpiration rates and stomatal conductance, but the mechanisms that are involved are elusive [90,102].

3.4. Cytokinin Effects on Growth

As cytokinins play key roles in root and shoot development they also participate in expression of growth and architectural traits that are required for tolerance of water-limiting conditions [113]. Cytokinins are well known to reduce root to shoot hypocotyl ratios [39,114,115], and one of the approaches for enhancing plants’ drought tolerance is to decrease cytokinin levels in order to modify root morphology and enhance root biomass [116]. Root-specific overexpression of CKX can also enhance root growth, nutrient uptake, and drought tolerance [106], as well as improving recovery after drought stress [116] without adverse effects on shoot growth. Similarly, one of the dehydration-responsive element binding factors in Malus (MdDREB6.2) activates the expression of MdCKX, mainly in roots, and overexpression of this factor can enhance drought tolerance [110]. Several studies indicate that not only quantitative features but also qualitative traits of root tissues could be important factors in cytokinin-regulated responses to water-limiting conditions, including the differentiation of vascular tissue [117] and lignification [116].

3.5. Cytokinin Crosstalk with Stress-Related Phytohormones

3.5.1. Abscisic Acid

Rapid accumulation of the phytohormone abscisic acid plays a crucial role in regulating plants’ defensive responses to drought stress, including stomatal closure, growth modulation, and synthesis of protective metabolites. It has been known for more than a decade that cytokinin and abscisic acid have antagonistic functions in diverse physiological processes, including stress tolerance, germination, and hypocotyl greening [95,118,119]. Cytokinin signalling has been shown to be dramatically inhibited by abscisic acid application [120,121] and cytokinin facilitates degradation of the abscisic acid signalling component transcription factor ABI5 [118]. It has been reported that under drought stress plants with decreased levels of cytokinin or attenuated cytokinin signalling have decreased levels of abscisic acid, but higher sensitivity to this stress-related hormone and greater drought tolerance [57,92,122]. However, elucidation of the molecular mechanism involved in this interaction has begun only recently. Experiments with a series of cytokinin and abscisic acid signalling mutants have demonstrated that cytokinin and abscisic acid interact directly through their signalling components, as plants constitutively expressing HA-Flag-ARR5 and arr5 loss-of-function mutants respectively showed increased and attenuated sensitivity to abscisic acid treatment [97]. ARR5 stability is promoted by phosphorylation catalysed by SnRK2 protein kinases that are key components of the abscisic acid signalling pathway. In contrast, type-B ARR1, 11, and 12 interact with these SnRK2s and repress their kinase activity, and the abscisic acid hypersensitivity of the triple mutant arr1,11,12 can be completely rescued by mutation of SnRK2s [97]. Interestingly, the same authors found that expression of ARR1ΔDDK (a constitutively activated form of ARR1), but not constitutive expression of ARR1-Myc, was associated with slight insensitivity to abscisic acid, suggesting that the modulation of ARR1’s phosphorylation status by cytokinin signalling may also be important. Since cytokinin is essential for normal growth of plants [10] the SnRK2-ARR regulatory module is clearly a recently discovered signalling hub that balances growth and defence in response to environmental cues.

3.5.2. Jasmonates

Jasmonic acid is known to play a role in drought tolerance [123,124]. Inter alia, drought-induced xylem differentiation is negatively and positively regulated by cytokinin and jasmonic acid, respectively, and jasmonic acid attenuates cytokinin signalling by repressing the cytokinin receptor AHK4 and stimulating expression of AHP6, a negative regulator of cytokinin signalling [117]. In addition, cytokinin may influence jasmonate metabolism. Ectopic expression of AtCKX1 in barley plants has been found to induce expression of lipoxygenases, which participate in the release of volatile compounds, including jasmonates [105], but an increase in jasmonic acid has also been observed in tobacco plants with highly increased levels of cytokinin [112].

4. Temperature and Cytokinin

Temperature is one of the most important abiotic factors influencing plants’ growth, development, productivity, and yields. Plants can only grow within taxa-specific temperature ranges, thus suboptimal temperatures cause stress, and temperature limits their geographical distributions. The mechanisms that are involved in temperature perception and signalling in plants are far from completely understood, but key aspects of associated morphological changes are clearly mediated by phytohormones.

4.1. Low Temperature Stress: Cold and Freezing

Most reported responses of cytokinin metabolism or signalling systems to low temperatures in plants are repressive [94,125,126,127,128], but there are some documented exceptions, notably cold-mediated upregulation of AHK3 [95]. However, the responses are complex, and roles of cytokinin and cytokinin signalling pathways in cold tolerance are unclear. Cold-induced attenuation of cytokinin signalling seems to impair plants’ tolerance of low temperature because the exogenous application of cytokinin significantly promotes cold tolerance in Arabidopsis [129,130,131]. Accordingly, recent hormonal analysis of Zoysia grass has shown that a genotype from relatively high latitude retained higher cytokinin levels during low-temperature treatment and exhibited higher freezing tolerance than a genotype from a lower latitude [128]. However, this seems to conflict with a reported negative role of AHK cytokinin receptors in cold tolerance [129]. The mechanisms whereby cytokinin could both promote cold tolerance and activate negative regulators of cold stress responses is unclear, but it seems to be at least partially independent of the cold-induced CBF/DREBs regulatory system [129].
Cold has also been shown to transiently activate expression of type-A ARRs in a cytokinin- and ethylene-dependent manner [129,130]. Mutation of ARR5, ARR6, and ARR7 leads to higher freezing tolerance [129], but the overexpression of ARR7 reportedly has both negative [129] and positive effects [130]. Results of overexpression studies indicate that other type-A ARRs [130] and ARR22, a cold-inducible type-C ARR [131], may also play positive roles in freezing tolerance. As shown by these conflicting results, the molecular mechanisms involved are unclear and further research is required. Besides ARRs, cytokinin response factors (CRFs) that act downstream of the primary cytokinin signalling pathway participate in responses to low temperature. More specifically, CRFs are induced by cold in Arabidopsis and tomato [130,132], and detailed analysis of Arabidopsis overexpressors and mutants has shown that CRF4 mediates freezing tolerance in non-acclimated plants [132], while CRF2 and CRF3 regulate lateral root development in response to cold stress [133]. Our meta-analysis revealed two novel candidates for interactive points in cytokinin-cold stress crosstalk: the MAP kinase MKK2, and the component of the ubiquitin-proteasome pathway, HOS1. The gene encoding HOS1 has a similar expression pattern to four and five genes that are involved in cytokinin metabolism and signalling, respectively (Figure 4). Cytokinin and its signalling evidently play important roles in cold stress responses, but various aspects of the molecular mechanism of their action regarding (for example) the duration of the period of cytokinin modulation prior to the stress require clarification

4.2. High Temperature and Heat Stress

Observed responses of Arabidopsis to heat stress treatments include a rapid but transient increase in active cytokinin contents [134,135]. A rapid proteomic heat-shock response that could be mimicked to some extent by cytokinin treatment at standard temperature has also been reported [136], indicating that cytokinin may play a role in temperature perception. Moreover, the accumulation of cytokinin has been observed in Pinus radiata under prolonged heat stress and in recovered plants [137,138]. Plants with increased levels of cytokinins show a higher accumulation of heat-shock proteins [107,139,140] and enhanced activity of the antioxidant system [88,112]. Accordingly, transgenic lines with inactivated components of cytokinin signalling pathways or reductions in pools of active cytokinin have displayed increased tolerance to high temperatures [141,142]. Further, analyses of temperature-induced hypocotyl growth in cytokinin-deficient transgenic plants and cytokinin receptor ahk double mutants have shown that impairment of the cytokinin pathway strongly inhibits growth at high temperatures [136]. This indicates that cytokinin could serve as a signal for thermomorphogenesis. It is also likely that a higher temperature sensitizes cytokinin signalling, which could explain why a transient increase in the active cytokinin pool is followed by its significant depletion [134,135], and downregulation in cytokinin metabolism genes and the expression of ARR-type A orthologs in strawberry (Fragaria vesca) [143,144]. It has also been proposed that heat stress-induced cytokinin depletion can promote stomatal closure, as this process is inhibited in plants with increased cytokinin levels [135].

5. Light Signalling and the Circadian Clock Interact with Cytokinin

As described in a recent review [145], soon after its discovery it was found that cytokinin promotes chlorophyll synthesis and chloroplast development. There is increasing evidence of direct interactions between cytokinin and light via the light photoreceptor phyB [146,147]. Moreover, cytokinin-mediated development in Arabidopsis is modulated by the expression of the sensor histidine kinase CKI1 (Cytokinin Independent-1), which is regulated by phyA (and thus light) via the phyA interacting factor (PIF3) and Circadian Clock Associated 1 (CCA1) [148]. Further, levels of the cytokinin pool in tobacco leaves vary diurnally, with the main peak occurring around midday [149], and a key component of the circadian clock in plants, Late Elongated Hypocotyl (LHY), modulates cytokinin levels in Populus trees [150]. Reductions in cytokinin status or sensitivity enhance circadian stress in Arabidopsis and cytokinin-deficient plants display a highly similar expression of clock output genes to that of clock mutants [151]. Light conditions may also influence contents of specific cytokinins, as recently demonstrated in detached leaf experiments [152]. Moreover, light-cytokinin interactions are not limited to cytokinin metabolism and components of the two-component cytokinin responsive pathway. They also influence a bZIP transcription factor, Elongated Hypocotyl 5 (HY5), which participates in photomorphogenesis [94,153]. Cytokinin is also apparently involved in photoprotection mechanisms as plants with deficiencies in cytokinin receptors or cytokinin signalling are more susceptible to light stress than wild-type counterparts [154,155]. To identify new candidate participants in light-cytokinin interactions, we subjected Arabidopsis transcriptomic expression profiles to association analysis. Data were collected from the publicly available database Thalemine (available online: http://apps.araport.org/thalemine/), then normalized, and degrees of similarity between expression patterns were visualized in a heatmap (Figure 5). In total, we tested similarities in expression profiles of 70 candidate cytokinin genes and 31 genes that were putatively involved in light signalling. The analysis revealed that 10 of the latter had similar expression patterns (>70%) to candidate cytokinin genes. The results confirmed the previously described relation between ARR and COP1, but also highlighted several novel putative interactions, including a connection between the UV-B receptor UVR8 and the AHP2 component of cytokinin signalling. This is consistent with a recent finding that cytokinin regulates UV-B-induced damage in tomato seedlings [156].

6. Summary

Generally, it can be concluded that cytokinin metabolism and signalling play important roles in abiotic stress tolerance and the manipulation of these processes in crops could be beneficial for sustainable agriculture. However, recent studies have mainly focused on global transcriptomic, proteomic and metabolomic changes in various plant species with modulated cytokinin levels [105,122,250]. Thus, further detailed analysis is required to confirm the importance of identified candidate genes/proteins and validate their roles in stress tolerance. Moreover, current models have substantial gaps. There is mounting evidence of intensive crosstalk in phytohormonal signalling, including redox and proteasome-ubiquitin pathways [251]. Thus, any disruption in a single phytohormone signalling pathway will probably affect the whole hormonome, but current limits in the sensitivity and spatiotemporal scope of analyses constrain our ability to detect all of the changes. Ongoing advances in hormonome analyses will undoubtedly improve our understanding [252], but another limitation is that most presented findings are based solely on transcriptomic analyses, in some cases supplemented with results of knocking out or overexpressing specific genes. Furthermore, posttranslational modifications play important roles in regulatory networks [253], and thus abiotic responses [254]. Thus, they must also be considered. Similarly, to fully understand phytohormonal interactions in abiotic stress responses, it will be crucial to integrate protein-protein interactions and the associated signalling hubs and networks [255].

Author Contributions

All authors (J.P., J.N., V.K., M.L., B.B., M.Č.) contributed to the analytical and systematic search of the literature. M.L. performed and interpreted results of meta analyses; J.P., J.N. and M.Č. reviewed and determined the design and structure of the article.

Acknowledgments

This research was partially funded by grant AF-IGA-IP-2018/030 (Internal Grant Agency of the Faculty of AgriSciences, Mendel University in Brno), the LQ1601 (CEITEC 2020) project (which received a financial contribution from the Ministry of Education, Youths and Sports of the CR in the form of special support through the National Programme for Sustainability II funds), and by the Ministry of Education, Youths and Sports of CR from European Regional Development Fund-Project “Centre for Experimental Plant Biology”: No. CZ.02.1.01/0.0/0.0/16_019/0000738. The authors thank Jan Zouhar for constructive comments on the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Crosstalk between abiotic stress signals and cytokinin. Summary of interactive points between cytokinin metabolism and signalling pathways (as currently modelled in Arabidopsis [5]) and abiotic stress response pathways. See corresponding sections of the text for details and references.
Figure 1. Crosstalk between abiotic stress signals and cytokinin. Summary of interactive points between cytokinin metabolism and signalling pathways (as currently modelled in Arabidopsis [5]) and abiotic stress response pathways. See corresponding sections of the text for details and references.
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Figure 2. Similarity of expression patterns of genes related to nutrient stress and genes involved in cytokinin metabolism or signalling. Asterisks indicate profile similarities >85%. The heatmap was generated using R software and available data from Araport [33].
Figure 2. Similarity of expression patterns of genes related to nutrient stress and genes involved in cytokinin metabolism or signalling. Asterisks indicate profile similarities >85%. The heatmap was generated using R software and available data from Araport [33].
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Figure 3. Similarity of expression patterns of genes related to xenobiotic stress and genes involved in cytokinin metabolism or signalling. Asterisks indicate profile similarities >85%. The heatmap was generated using R software and available data from Araport [33].
Figure 3. Similarity of expression patterns of genes related to xenobiotic stress and genes involved in cytokinin metabolism or signalling. Asterisks indicate profile similarities >85%. The heatmap was generated using R software and available data from Araport [33].
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Figure 4. Similarity of expression patterns of genes related to temperature/drought stress and genes involved in cytokinin metabolism or signalling. Asterisks indicate profile similarities >85%. The heatmap was generated using R software and available data from Araport [33].
Figure 4. Similarity of expression patterns of genes related to temperature/drought stress and genes involved in cytokinin metabolism or signalling. Asterisks indicate profile similarities >85%. The heatmap was generated using R software and available data from Araport [33].
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Figure 5. Heatmap showing degrees of similarity between expression profiles of cytokinin (signalling and metabolism) genes and genes involved in light perception. The heatmap was generated using R software and data available from Araport [33]. Asterisks indicate >70% similarity.
Figure 5. Heatmap showing degrees of similarity between expression profiles of cytokinin (signalling and metabolism) genes and genes involved in light perception. The heatmap was generated using R software and data available from Araport [33]. Asterisks indicate >70% similarity.
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Table
Table 1. List of all abiotic stress-related genes, with references, and their putative interactions with cytokinin according to the expression profile analysis outlined in Figure 2, Figure 3 and Figure 4. Genes in bold indicate profile similarities >85% to cytokinin-related genes, and numbers indicate the number of detected co-expressed cytokinin signalling/metabolism genes.
Table 1. List of all abiotic stress-related genes, with references, and their putative interactions with cytokinin according to the expression profile analysis outlined in Figure 2, Figure 3 and Figure 4. Genes in bold indicate profile similarities >85% to cytokinin-related genes, and numbers indicate the number of detected co-expressed cytokinin signalling/metabolism genes.
Gene NameAGI CodeUniProt Protein NameSignificant Co-Expression with Cytokinin Signalling/Metabolism GenesReferences
NITROGEN
NPF6.3AT1G12110Protein NRT1/PTR FAMILY 6.3 [157]
NRT2.1AT1G08090High-affinity nitrate transporter 2.1 [158]
NRT2.2AT1G08100High-affinity nitrate transporter 2.2 [157]
NRT2.4AT5G60770High affinity nitrate transporter 2.4 [159,160]
NRT2.5AT1G12940High affinity nitrate transporter 2.5 [13,157,161]
AMT1-1AT4G13510Ammonium transporter 1 member 1 [157]
AMT1-5AT3G24290Putative ammonium transporter 1 member 5 [161,162]
GDH2AT5G07440Glutamate dehydrogenase 2 [157]
GSH3AT3G03910Probable glutamate dehydrogenase 3 [157]
GLN2AT5G35630Glutamine synthetase2/4[157,158]
GLU2AT2G41220Ferredoxin-dependent glutamate synthase 2 [163]
NIA1AT1G77760Nitrate reductase [NADH] 1 [13,158]
NIA2AT1G37130Nitrate reductase [NADH] 2 [157]
NIR1AT2G15620Ferredoxin–nitrite reductase1/0[13,158]
UMP1AT5G40850Urophorphyrin methylase 1 [13,157,158]
GLN1-1AT5G37600Glutamine synthetase cytosolic isozyme 1-1 [159,164]
GLN1-4AT5G16570Glutamine synthetase cytosolic isozyme 1-40/1[157,164]
At3g16150AT3G16150Probable isoaspartyl peptidase/l-asparaginase 2 [157,159]
ASN2AT5G65010Asparagine synthetase [glutamine-hydrolyzing] 2 [22,157]
ASN3AT5G10240Asparagine synthetase [glutamine-hydrolyzing] 31/1[165]
At5g13110AT5G13110Glucose-6-phosphate 1-dehydrogenase 22/1[157,158]
At1g24280AT1G24280Glucose-6-phosphate 1-dehydrogenase 31/2[22,158]
UPS1AT2G03590Ureide permease 1 [159]
AT4G39795AT4G39795Uncharacterized protein [159]
RFNR1AT4G05390Ferredoxin–NADP reductase [14,158]
RFNR2AT1G30510Ferredoxin–NADP reductase1/1[158]
GSTF14AT1G49860Glutathione S-transferase F14 [158]
BT5AT4G37610BTB/POZ and TAZ domain-containing protein 5 [158]
CCA1AT2G46830Protein CCA1 [157]
TGA1AT5G65210Transcription factor TGA1 [166]
TGA4AT5G10030Transcription factor TGA4 [166]
NLP3AT4G38340Protein NLP31/0[167]
NLP5AT1G76350Protein NLP5 [167]
NLP7AT4G24020Protein NLP7 [167]
HHO1AT3G25790Transcription factor HHO10/1[158,160]
HRS1AT1G13300Transcription factor HRS1 [158,160]
HHO3AT1G25550Transcription factor HHO3 [22,158,160]
LBD37AT5G67420LOB domain-containing protein 37 [14,158,168]
LBD38AT3G49940LOB domain-containing protein 38 [14,158,168]
LBD39AT4G37540LOB domain-containing protein 390/1[158,168]
CIPK3AT2G26980CBL-interacting serine/threonine-protein kinase 3 [158]
CIPK13AT2G34180CBL-interacting serine/threonine-protein kinase 13 [157]
AOAT5G14760l-aspartate oxidase [158]
PHOSPHORUS
PHO1AT3G23430Phosphate transporter PHO10/2[38]
PHO1-H1AT1G68740Phosphate transporter PHO1 homolog 10/1[169]
PHF1AT3G52190SEC12-like protein 10/3[169]
PHT1-1AT5G43350Inorganic phosphate transporter 1-1 [170,171]
PHT1-2AT5G43370Probable inorganic phosphate transporter 1-2 [171,172]
PHT1-3AT5G43360Probable inorganic phosphate transporter 1-31/1[38,171]
PHT1-4AT2G38940Inorganic phosphate transporter 1-41/0[171,172]
PHT1-5AT2G32830Probable inorganic phosphate transporter 1-51/0[170,171]
PHT1-6AT5G43340Probable inorganic phosphate transporter 1-60/1[172]
PHT1-7AT3G54700Probable inorganic phosphate transporter 1-7 [173]
PHT1-8AT1G20860Probable inorganic phosphate transporter 1-8 [172,173]
PHT1-9AT1G76430Probable inorganic phosphate transporter 1-91/1[172,173]
PHT2-1AT3G26570Inorganic phosphate transporter 2-1 [170,172]
SPX1AT5G20150SPX domain-containing protein 1 [169,174]
SPX2AT2G26660SPX domain-containing protein 20/2[174]
SPX3AT2G45130SPX domain-containing protein 3 [38]
IPS1AT3G09922INDUCED BY PHOSPHATE STARVATION1 [169,174]
F12E4_330AT5G03545At5g03545 [169]
ACP5AT5G27200Acyl carrier protein 5 [38]
RNS1AT2G02990Ribonuclease 1 [169,170]
SQD2AT5G01220Sulfoquinovosyl transferase SQD2 [169]
PAP10AT2G16430Purple acid phosphatase 10 [38]
PAP6AT1G56360Purple acid phosphatase 6 [38]
At4g19770AT4G19770Glycosyl hydrolase family protein with chitinase insertion domain-containing protein [38]
PUB35AT4G25160U-box domain-containing protein 35 [38]
GDPD3AT5G43300Glycerophosphodiester phosphodiesterase GDPD3 [38]
ETC3AT4G01060MYB-like transcription factor ETC3 [38]
SULPHUR
SULTR1;1AT4G08620Sulfate transporter 1.1 [175,176]
SULTR2;1AT5G10180Sulfate transporter 2.1 [175,176]
SULTR4;1AT5G13550Sulfate transporter 4.1 [177,178]
SULTR4;2AT3G12520Probable sulfate transporter 4.2 [178,179,180,181]
APS3AT4G14680ATP-sulfurylase 3 [176,178]
APR1AT4G046105′-adenylylsulfate reductase 1 [176,178]
APR2AT1G621805′-adenylylsulfate reductase 20/1[178]
APR3AT4G219905′-adenylylsulfate reductase 30/1[178,180]
SAT4AT4G35640Serine acetyltransferase 4 [181,182]
BGLU28AT2G44460Beta-glucosidase 28 [179,180]
BGLU30AT3G60140Beta-glucosidase 30 [180,182]
SDI1AT5G48850Protein SULFUR DEFICIENCY-INDUCED 1 [178,179]
SDI2AT1G04770Protein SULFUR DEFICIENCY-INDUCED 2 [176,178]
SHM7AT1G36370Serine hydroxymethyltransferase 7 [178,180]
GGCT2;1AT5G26220Gamma-glutamylcyclotransferase 2-1 [178,180,182]
LSU1AT3G49580Protein RESPONSE TO LOW SULFUR 1 [178,180]
LSU2AT5G24660Protein RESPONSE TO LOW SULFUR 2 [178,180,182]
At3g05400AT3G05400Sugar transporter ERD6-like 12 [180,182]
At4g31330AT4G31330Protein of unknown function0/2[180,182]
SIP1-2AT5G18290Probable aquaporin SIP1-22/1[180]
At5g40670AT5G40670Cystinosin homolog [180]
At1g75290AT1G75290NAD [180]
NSP5AT5G48180Nitrile-specifier protein 5 [180]
AVT6CAT3G56200Amino acid transporter AVT6C [178,180]
NFYA2AT3G05690Nuclear transcription factor Y subunit A-2 [180]
BZIP1AT5G49450Basic leucine zipper 1 [180]
RVE2AT5G37260Homeodomain-like superfamily protein [180]
POTASSIUM
POT5AT4G13420Potassium transporter 5 [182,183]
POT4AT3G02050Potassium transporter 42/2[183]
AKT1AT2G26650Potassium channel AKT1 [184,185]
RBOHCAT5G51060Respiratory burst oxidase homolog protein C [183]
CIPK23AT1G30270CBL-interacting serine/threonine-protein kinase 23 [183,186]
TGG1AT5G26000Myrosinase 1 [182]
TGG2AT5G25980Myrosinase 2 [182]
POT6AT1G70300Potassium transporter 6 [187]
POT8AT5G14880Potassium transporter 81/2[184,187]
KEA5AT5G51710K+ efflux antiporter 50/2[183]
KAT3AT4G32650Potassium channel KAT3 [184]
SKORAT3G02850Potassium channel SKOR [184,188,189]
AKT2AT4G22200Potassium channel AKT2/30/1[189]
POT3AT4G23640Potassium transporter 32/0[190]
POT7AT5G09400Potassium transporter 72/3[191]
CBL1AT4G17615Calcineurin B-like protein 1 [189]
CBL9AT5G47100Calcineurin B-like protein 90/1[189]
CBL10AT4G33000Calcineurin B-like protein 10 [183]
TCH3AT2G41100Calcium-binding EF hand family protein [192]
ERF73AT1G72360Integrase-type DNA-binding superfamily protein [183]
IRON
AXX17_At1g47400AT1G47400Uncharacterized protein [182,193]
At1g47395AT1G47395At1g47390 [182]
AT2G14247AT2G14247Expressed protein [182]
At1g13609AT1G13609Defensin-like [182]
IRT1AT4G19690Fe2+ transport protein 1 [182,193,194]
F17A17.6AT3G07720AT3g07720/F17A17_6 [182,193,194]
MTPA2AT3G58810Metal tolerance protein A2 [193,194]
MJM20.4AT3G129002-oxoglutarate [193,194]
F21F14.100AT3G61930Uncharacterized protein At3g61930/F21F14_100 [193,194]
COPT2AT3G46900Copper transporter 2 [193,194]
CYP82C4AT4G31940Cytochrome P450 82C4 [193]
GLP4AT1G09560Germin-like protein subfamily 2 member 1 [193,194]
F17A9.4AT3G06890At3g06890 [193,194]
UGT72E1AT3G50740UDP-glycosyltransferase 72E1 [193,194]
ORG3AT3G56980Transcription factor ORG3 [182,193,194]
MYB72AT1G56160Transcription factor MYB72 [193,194]
MTPC3AT3G58060Putative metal tolerance protein C3 [193,194]
FITAT2G28160Transcription factor FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR [194,195]
BHLH47AT3G47640Transcription factor bHLH472/1[193,195]
BHLH101AT5G04150Transcription factor bHLH101 [182,193]
NAS4AT1G56430Probable nicotianamine synthase 4 [182,193]
OPT3AT4G16370Oligopeptide transporter 3 [195,196]
CGLD27AT5G67370Protein CONSERVED IN THE GREEN LINEAGE AND DIATOMS 27 [182]
FRO2AT1G01580Ferric reduction oxidase 2 [182]
FRO3AT1G23020Ferric reduction oxidase 3 [193,195]
AHA2AT4G30190Plasma membrane ATPase [195]
NRAMP4AT5G67330Metal transporter Nramp41/1[193,195]
FER1AT5G01600Ferritin-1 [193,194]
ABCI8AT4G04770UPF0051 protein ABCI8 [193,194]
At2g36885AT2G36885Translation initiation factor0/1[193,194,195]
APXSAT4G08390Stromal ascorbate peroxidase1/1[193,194]
LAC7AT3G09220Laccase-7 [193,194,195]
IRT3AT1G60960Fe2+ transport protein 3, chloroplastic1/1[193]
At4g08300AT4G08300WAT1-related protein At4g08300 [182]
FRO4AT5G23980Ferric reduction oxidase 4 [185]
BORON
BOR1AT2G47160Boron transporter 1 [197]
BOR4AT1G15460Boron transporter 41/1[198]
TEMPERATURE/DROUGHT
RD29AAT5G52310Low-temperature-induced 78 kDa protein [141,199,200]
KIN1AT5G15960Stress-induced protein KIN1 [201,202]
KIN2AT5G15970Stress-induced protein KIN2 [203,204]
COR15AAT2G42540Protein COLD-REGULATED 15A [200,201,202]
COR47AT1G20440Dehydrin COR47 [201,202]
ERD10AT1G20450Dehydrin ERD10 [201,202]
ERD7AT2G17840Protein EARLY-RESPONSIVE TO DEHYDRATION 7 [201,202,205]
At1g30790AT1G30790F-box protein At1g307900/2[205]
MKK2AT4G29810Mitogen-activated protein kinase kinase 2 [206]
RAB18AT5G66400Dehydrin Rab18 [207,208,209]
LTI65/RD29BAT5G52300Low-temperature-induced 65 kDa protein [129,199,200]
RD22AT5G25610BURP domain protein RD22 [207,209]
HOS1AT2G39810E3 ubiquitin-protein ligase HOS14/3[203,210]
DREB1BAT4G25490Dehydration-responsive element-binding protein 1B [201,202]
DREB1CAT4G25470Dehydration-responsive element-binding protein 1C [201,202,209]
DREB1AAT4G25480Dehydration-responsive element-binding protein 1A [201,202]
RABC1AT1G43890Ras-related protein RABC10/2[202]
CLPDAT5G51070Chaperone protein ClpD [209,211]
SWEET15AT5G13170Bidirectional sugar transporter SWEET15 [40,209]
P5CSAAT2G39800Delta-1-pyrroline-5-carboxylate synthase A [40,209]
ABI1AT4G26080Protein phosphatase 2C 56 [209]
DREB2AAT5G05410Dehydration-responsive element-binding protein 2A [209,212]
NCED3AT3G144409-cis-epoxycarotenoid dioxygenase NCED3 [200,209]
ABF3AT4G34000ABSCISIC ACID-INSENSITIVE 5-like protein 6 [209,213]
PP2CAAT3G11410Protein phosphatase 2C 372/2[200,209,214]
PXG3/RD20AT2G33380Probable peroxygenase 3 [200,209,211]
LEA7AT1G52690Late embryogenesis abundant protein 7 [209,215]
LEA29AT3G15670Late embryogenesis abundant protein 29 [40]
At3g17520AT3G17520Late embryogenesis abundant protein [208,209]
NAC072AT4G27410NAC domain-containing protein 72 [208,209]
MBF1CAT3G24500Multiprotein-bridging factor 1c [216,217]
HSFA2AT2G26150Heat stress transcription factor A-2 [217,218,219]
HSA32AT4G21320Protein HEAT-STRESS-ASSOCIATED 32 [216,217,218]
CLPB1AT1G74310Chaperone protein ClpB1 [216,217,218]
CLPB3AT5G15450Chaperone protein ClpB3 [216,218]
HSFB2AAT5G62020Heat stress transcription factor B-2a [216,219]
HSFA7AAT3G51910Heat stress transcription factor A-7a [217,218,219]
HSP90-1AT5G52640Heat shock protein 90-1 [216,217,218]
HSP90-2AT5G56030Heat shock protein 90-2 [216,217]
At2g20560AT2G20560At2g20560/T13C7.15 [216,217,218]
HSFB1AT4G36990Heat stress transcription factor B-1 [216,217,218]
HSP23.6AT4G2520023.6 kDa heat shock protein [217,218]
HSP18.1AT5G5972018.1 kDa class I heat shock protein [217,218]
HSP17.4BAT1G5405017.4 kDa class III heat shock protein [216,217]
MED37CAT3G12580Probable mediator of RNA polymerase II transcription subunit 37c [217,220]
HSP70-5AT1G16030Heat shock 70 kDa protein 5 [217,218,220]
HSP70-10AT5G09590Heat shock 70 kDa protein 10 [216,217]
GOLS1AT2G47180Galactinol synthase 1 [216,217,218]
APX2AT3G09640L-ascorbate peroxidase 2 [217,218]
ERDJ3AAT3G08970DnaJ protein ERDJ3A [216,217]
HSP90-6AT3G07770Heat shock protein 90-62/0[216,217]
HSP90-4AT5G56000Heat shock protein 90-4 [216,217]
HSP70-8AT2G32120Heat shock 70 kDa protein 8 [216,217]
MED37DAT5G02490Probable mediator of RNA polymerase II transcription subunit 37c [216,217]
HSP70-3AT3G09440Heat shock 70 kDa protein 3 [216,217]
HSP70-15AT1G79920Heat shock 70 kDa protein 150/2[216,217]
HSP90-5AT2G04030Heat shock protein 90-50/1[216,217]
XENOBIOTIC STRESS
GSH1AT4G23100Glutamate–cysteine ligase [221,222]
GSH2AT5G27380Glutathione synthetase [221,222]
PCS1AT5G44070Glutathione gamma-glutamylcysteinyltransferase 1 [221,222]
MAN3AT3G10890Mannan endo-1 [223]
ZAT6AT5G04340Zinc finger protein ZAT6 [223]
PCR1AT1G14880Protein PLANT CADMIUM RESISTANCE 1 [224]
HMA3AT4G30120Putative inactive cadmium/zinc-transporting ATPase HMA3 [225,226]
HMA4AT2G19110Putative cadmium/zinc-transporting ATPase HMA42/1[227]
HSFA4AAT4G18880Heat stress transcription factor A-4a [228]
FC1AT5G26030Ferrochelatase-1 [222]
HMT-1AT3G25900Homocysteine S-methyltransferase 12/2[229]
MT1AAT1G07600Metallothionein-like protein 1A1/4[230]
NRAMP5AT4G18790Metal transporter Nramp52/2[226,231]
ABCG36AT1G59870ABC transporter G family member 36 [232]
ABCB25AT5G58270ABC transporter B family member 254/3[233]
ABCC1AT1G30400ABC transporter C family member 14/2[226,234,235]
ABCC2AT2G34660ABC transporter C family member 210/7[226,234,235]
HAC1AT2G21045Protein HIGH ARSENIC CONTENT 11/1[236]
ALMT1AT1G08430Aluminum-activated malate transporter 1 [237,238]
ALS3AT2G37330Protein ALUMINUM SENSITIVE 32/4[237,239]
STOP1AT1G34370Protein SENSITIVE TO PROTON RHIZOTOXICITY 10/1[237,239]
CYP81D11AT3G28740Cytochrome P450 81D11 [240,241,242,243]
CYP710A1AT2G34500Cytochrome P450 710A1 [82,244,245]
CYP81D8AT4G37370Cytochrome P450 [81,243,244,245]
UGT73B2AT4G34135UDP-glucosyl transferase 73B2 [241,242,244]
UGT73B3AT4G34131UDP-glycosyltransferase 73B3 [242,244]
UGT73B4AT2G15490UDP-glycosyltransferase 73B4 [241,242,244]
UGT73C1AT2G36750UDP-glycosyltransferase 73C1 [241]
GSTU3AT2G29470Glutathione S-transferase U3 [241,244]
GSTU10AT1G74590Glutathione S-transferase U10 [82,243,246]
GSTU19AT1G78380Glutathione S-transferase U192/3[243,247]
GSTU24AT1G17170Glutathione S-transferase U24 [240,241,242,243]
GSTU25AT1G17180Glutathione S-transferase U25 [241,242,243,244]
GSTU26AT1G17190Glutathione S-transferase U26 [248]
GGT4AT4G29210Glutathione hydrolase 31/0[249]
ABCC3AT3G13080ABC transporter C family member 3 [244]
ABCI21AT5G44110ABC transporter I family member 21 [242,243]
DTX1AT2G04040Protein DETOXIFICATION 1 [243,245]
DTX3AT2G04050Protein DETOXIFICATION 3 [243,245]
DTX4AT2G04070Protein DETOXIFICATION 4 [241,245]
CYP710A2AT2G34490Cytochrome P450 710A2 [82]
DHAR2AT1G75270Glutathione S-transferase DHAR21/0[243,244]
DHAR3AT5G16710Glutathione S-transferase DHAR32/0[243]
GSTU4AT2G29460Glutathione S-transferase U4 [241,244]
UGT74F2AT2G43820UDP-glycosyltransferase 74F2 [244,246]
UGT73C6AT2G36790UDP-glycosyltransferase 73C60/1[241,245]
UGT74E2AT1G05680UDP-glycosyltransferase 74E2 [241,245]
UGT73B5AT2G15480UDP-glycosyltransferase 73B5 [241,244]
UGT75B1AT1G05560UDP-glycosyltransferase 75B1 [241,244]
CYP81F2AT5G57220Cytochrome P450 81F2 [241]
CYP87A2AT1G12740Photosynthetic NDH subunit of lumenal location 51/1[240]
GSTF7AT1G02920Glutathione S-transferase F7 [243]
GSTF6AT1G02930Glutathione S-transferase F6 [243,246]
ABCB15AT3G28345ABC transporter B family member 15 [242]

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MDPI and ACS Style

Pavlů, J.; Novák, J.; Koukalová, V.; Luklová, M.; Brzobohatý, B.; Černý, M. Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways. Int. J. Mol. Sci. 2018, 19, 2450. https://doi.org/10.3390/ijms19082450

AMA Style

Pavlů J, Novák J, Koukalová V, Luklová M, Brzobohatý B, Černý M. Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways. International Journal of Molecular Sciences. 2018; 19(8):2450. https://doi.org/10.3390/ijms19082450

Chicago/Turabian Style

Pavlů, Jaroslav, Jan Novák, Vladěna Koukalová, Markéta Luklová, Břetislav Brzobohatý, and Martin Černý. 2018. "Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways" International Journal of Molecular Sciences 19, no. 8: 2450. https://doi.org/10.3390/ijms19082450

APA Style

Pavlů, J., Novák, J., Koukalová, V., Luklová, M., Brzobohatý, B., & Černý, M. (2018). Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways. International Journal of Molecular Sciences, 19(8), 2450. https://doi.org/10.3390/ijms19082450

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