Roles of Cytokinins in Plants and Their Response to Environmental Stimuli

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (15 March 2020) | Viewed by 36238

Special Issue Editors


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Guest Editor
Trent University, Department of Biology, Peterborough, Canada
Interests: plant physiological and molecular development; physiological ecology; hormone signaling; cytokinins; biotic and abiotic interactions with plants

E-Mail Website
Guest Editor
Department of Biology, Trent University, Peterborough, Canada
Interests: phytohormone profiling by HPLC-MS/MS; cytokinin role in plant interactions with environment; plant growth promoting bacteria

Special Issue Information

Dear Colleagues,

Cytokinins (CKs) are adenine-derived, small-molecule plant growth regulators that control aspects of almost all plant growth and development processes. Internally, CKs play significant roles in plant cell division, nutrient allocation, and photosynthetic performance, and they are also detection and signalling agents for plant responses to the environmental challenges. CK functions in plant metabolism include plant adaptations to various abiotic stresses as well as their regulatory role in plant interactions with biotic components of the environment. Interestingly, CK biosynthesis is not exclusive to plants. New genetic and chemical approaches have revealed that both beneficial (symbiotic microorganisms) and detrimental (pathogenic bacteria, fungi, or insects) non-plant biota can secrete these phytohormones to purposefully modify plant metabolism. Therefore, while many open questions remain about how CKs are actively utilized by plants and plant-interacting organisms, CK roles should be seen more broadly, as signalling molecules for which effects range from within cells to as far as interkingdom relationships.

In this Special Issue of Plants, authors are invited to publish reviews, mini-reviews, and research articles on several aspects of cytokinin biosynthesis, metabolism, and functions within plants and among plant-associated organisms. This Special Issue welcomes advances in towards knowledge about multilayered mechanisms of cytokinin contribution both within plants and those involved in plant interactions with biotic and abiotic challenges faced during the plant life cycle.

Prof. R.J. Neil Emery
Dr. Anna Kisiala
Guest Editors

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Keywords

  • cytokinin
  • biosynthesis and metabolism
  • structure–role
  • hormonal response
  • abiotic stress
  • biotic interactions
  • interkingdom signaling

Published Papers (7 papers)

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Editorial

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4 pages, 192 KiB  
Editorial
The Roles of Cytokinins in Plants and Their Response to Environmental Stimuli
by R. J. Neil Emery and Anna Kisiala
Plants 2020, 9(9), 1158; https://doi.org/10.3390/plants9091158 - 08 Sep 2020
Cited by 8 | Viewed by 3202
Abstract
Cytokinins (CKs) are adenine-derived, small-molecule plant growth regulators that control aspects of almost all plant growth and development processes. Internally, CKs play significant roles in plant cell division, nutrient allocation, and photosynthetic performance, and they are also detection and signaling agents for plant [...] Read more.
Cytokinins (CKs) are adenine-derived, small-molecule plant growth regulators that control aspects of almost all plant growth and development processes. Internally, CKs play significant roles in plant cell division, nutrient allocation, and photosynthetic performance, and they are also detection and signaling agents for plant responses to the environmental challenges. CK functions in plant metabolism include plant adaptations to various abiotic stresses as well as their regulatory role in plant interactions with biotic components of the environment. Interestingly, CK biosynthesis is not exclusive to plants. New genetic and chemical approaches have revealed that both beneficial (symbiotic microorganisms) and detrimental (pathogenic bacteria, fungi, or insects) non-plant biota can secrete these phytohormones to purposefully modify plant metabolism. Therefore, while many open questions remain about how CKs are actively utilized by plants and plant-interacting organisms, CK roles should be seen more broadly, as signaling molecules for which effects range from within cells to as far as interkingdom relationships. The papers in this Special Issue highlight several aspects of CK biosynthesis, metabolism, and functions within plants and among plant-associated organisms, typifying the extensive range of roles played by these signaling molecules. The collection of papers represents new examples for CK researchers to consider advancing the growing range of topics related to how CKs mediate responses to many kinds of environmental stimuli and stresses. Full article

Research

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18 pages, 3011 KiB  
Article
Heterologous Expression of a Soybean Gene RR34 Conferred Improved Drought Resistance of Transgenic Arabidopsis
by Duong Hoang Trong Nghia, Nguyen Nguyen Chuong, Xuan Lan Thi Hoang, Nguyen Cao Nguyen, Nguyen Huu Cam Tu, Nguyen Van Gia Huy, Bui Thi Thanh Ha, Thai Nguyen Hoang Nam, Nguyen Binh Anh Thu, Lam-Son Phan Tran and Nguyen Phuong Thao
Plants 2020, 9(4), 494; https://doi.org/10.3390/plants9040494 - 12 Apr 2020
Cited by 6 | Viewed by 4324
Abstract
Two-component systems (TCSs) have been identified as participants in mediating plant response to water deficit. Nevertheless, insights of their contribution to plant drought responses and associated regulatory mechanisms remain limited. Herein, a soybean response regulator (RR) gene RR34, which is the potential [...] Read more.
Two-component systems (TCSs) have been identified as participants in mediating plant response to water deficit. Nevertheless, insights of their contribution to plant drought responses and associated regulatory mechanisms remain limited. Herein, a soybean response regulator (RR) gene RR34, which is the potential drought-responsive downstream member of a TCS, was ectopically expressed in the model plant Arabidopsis for the analysis of its biological roles in drought stress response. Results from the survival test revealed outstanding recovery ratios of 52%–53% in the examined transgenic lines compared with 28% of the wild-type plants. Additionally, remarkedly lower water loss rates in detached leaves as well as enhanced antioxidant enzyme activities of catalase and superoxide dismutase were observed in the transgenic group. Further transcriptional analysis of a subset of drought-responsive genes demonstrated higher expression in GmRR34-transgenic plants upon exposure to drought, including abscisic acid (ABA)-related genes NCED3, OST1, ABI5, and RAB18. These ectopic expression lines also displayed hypersensitivity to ABA treatment at germination and post-germination stages. Collectively, these findings indicated the ABA-associated mode of action of GmRR34 in conferring better plant performance under the adverse drought conditions. Full article
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20 pages, 1969 KiB  
Article
Exogenous Kinetin Promotes the Nonenzymatic Antioxidant System and Photosynthetic Activity of Coffee (Coffea arabica L.) Plants Under Cold Stress Conditions
by Robert Acidri, Yumiko Sawai, Yuko Sugimoto, Takuo Handa, Daisuke Sasagawa, Tsugiyaki Masunaga, Sadahiro Yamamoto and Eiji Nishihara
Plants 2020, 9(2), 281; https://doi.org/10.3390/plants9020281 - 21 Feb 2020
Cited by 23 | Viewed by 3857
Abstract
Coffee plants are seasonally exposed to low chilling temperatures in many coffee-producing regions. In this study, we investigated the ameliorative effects of kinetin—a cytokinin elicitor compound on the nonenzymatic antioxidants and the photosynthetic physiology of young coffee plants subjected to cold stress conditions. [...] Read more.
Coffee plants are seasonally exposed to low chilling temperatures in many coffee-producing regions. In this study, we investigated the ameliorative effects of kinetin—a cytokinin elicitor compound on the nonenzymatic antioxidants and the photosynthetic physiology of young coffee plants subjected to cold stress conditions. Although net CO2 assimilation rates were not significantly affected amongst the treatments, the subjection of coffee plants to cold stress conditions caused low gas exchanges and photosynthetic efficiency, which was accompanied by membrane disintegration and the breakdown of chlorophyll pigments. Kinetin treatment, on the other hand, maintained a higher intercellular-to-ambient CO2 concentration ratio with concomitant improvement in stomatal conductance and mesophyll efficiency. Moreover, the leaves of kinetin-treated plants maintained slightly higher photochemical quenching (qP) and open photosystem II centers (qL), which was accompanied by higher electron transfer rates (ETRs) compared to their non-treated counterparts under cold stress conditions. The exogenous foliar application of kinetin also stimulated the metabolism of caffeine, trigonelline, 5-caffeoylquinic acid, mangiferin, anthocyanins and total phenolic content. The contents of these nonenzymatic antioxidants were highest under cold stress conditions in kinetin-treated plants than during optimal conditions. Our results further indicated that the exogenous application of kinetin increased the total radical scavenging capacity of coffee plants. Therefore, the exogenous application of kinetin has the potential to reinforce antioxidant capacity, as well as modulate the decline in photosynthetic productivity resulting in improved tolerance under cold stress conditions. Full article
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23 pages, 2425 KiB  
Article
Cytokinins Are Abundant and Widespread among Insect Species
by Peter Andreas, Anna Kisiala, R. J. Neil Emery, Rosemarie De Clerck-Floate, John F. Tooker, Peter W. Price, Donald G. Miller III, Ming-Shun Chen and Edward F. Connor
Plants 2020, 9(2), 208; https://doi.org/10.3390/plants9020208 - 06 Feb 2020
Cited by 31 | Viewed by 7131
Abstract
Cytokinins (CKs) are a class of compounds that have long been thought to be exclusively plant growth regulators. Interestingly, some species of phytopathogenic bacteria and fungi have been shown to, and gall-inducing insects have been hypothesized to, produce CKs and use them to [...] Read more.
Cytokinins (CKs) are a class of compounds that have long been thought to be exclusively plant growth regulators. Interestingly, some species of phytopathogenic bacteria and fungi have been shown to, and gall-inducing insects have been hypothesized to, produce CKs and use them to manipulate their host plants. We used high performance liquid chromatography-electrospray ionization tandem mass spectrometry (HPLC-MS/MS) to examine concentrations of a wide range of CKs in 17 species of phytophagous insects, including gall- and non-gall-inducing species from all six orders of Insecta that contain species known to induce galls: Thysanoptera, Hemiptera, Lepidoptera, Coleoptera, Diptera, and Hymenoptera. We found CKs in all six orders of insects, and they were not associated exclusively with gall-inducing species. We detected 24 different CK analytes, varying in their chemical structure and biological activity. Isoprenoid precursor nucleotide and riboside forms of trans-zeatin (tZ) and isopentenyladenine (iP) were most abundant and widespread across the surveyed insect species. Notably, the observed concentrations of CKs often markedly exceeded those reported in plants suggesting that insects are synthesizing CKs rather than obtaining them from the host plant via tissue consumption, compound sequestration, and bioaccumulation. These findings support insect-derived CKs as means for gall-inducing insects to manipulate their host plant to facilitate cell proliferation, and for both gall- and non-gall-inducing insects to modify nutrient flux and plant defenses during herbivory. Furthermore, wide distribution of CKs across phytophagous insects, including non-gall-inducing species, suggests that insect-borne CKs could be involved in manipulation of source-sink mechanisms of nutrient allocation to sustain the feeding site and altering plant defensive responses, rather than solely gall induction. Given the absence of any evidence for genes in the de novo CK biosynthesis pathway in insects, we postulate that the tRNA-ipt pathway is responsible for CK production. However, the unusually high concentrations of CKs in insects, and the tendency toward dominance of their CK profiles by tZ and iP suggest that the tRNA-ipt pathway functions differently and substantially more efficiently in insects than in plants. Full article
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Review

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19 pages, 2278 KiB  
Review
Role and Regulation of Cytokinins in Plant Response to Drought Stress
by Nguyen Ngoc Hai, Nguyen Nguyen Chuong, Nguyen Huu Cam Tu, Anna Kisiala, Xuan Lan Thi Hoang and Nguyen Phuong Thao
Plants 2020, 9(4), 422; https://doi.org/10.3390/plants9040422 - 31 Mar 2020
Cited by 75 | Viewed by 10404
Abstract
Cytokinins (CKs) are key phytohormones that not only regulate plant growth and development but also mediate plant tolerance to drought stress. Recent advances in genome-wide association studies coupled with in planta characterization have opened new avenues to investigate the drought-responsive expression of CK [...] Read more.
Cytokinins (CKs) are key phytohormones that not only regulate plant growth and development but also mediate plant tolerance to drought stress. Recent advances in genome-wide association studies coupled with in planta characterization have opened new avenues to investigate the drought-responsive expression of CK metabolic and signaling genes, as well as their functions in plant adaptation to drought. Under water deficit, CK signaling has evolved as an inter-cellular communication network which is essential to crosstalk with other types of phytohormones and their regulating pathways in mediating plant stress response. In this review, we revise the current understanding of CK involvement in drought stress tolerance. Particularly, a genetic framework for CK signaling and CK crosstalk with abscisic acid (ABA) in the precise monitoring of drought responses is proposed. In addition, the potential of endogenous CK alteration in crops towards developing drought-tolerant crops is also discussed. Full article
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Other

4 pages, 373 KiB  
Commentary
Virulent Rhodococcus fascians Produce Unique Methylated Cytokinins
by Paula Elizabeth Jameson
Plants 2019, 8(12), 582; https://doi.org/10.3390/plants8120582 - 07 Dec 2019
Cited by 5 | Viewed by 2841
Abstract
Some strains of Rhodococcus fascians exist only as epiphytes on the plant surface whereas others can become endophytic and cause various abnormalities including the release of multiple buds and reduced root growth. The abnormalities reflect the action of cytokinin. The strains that can [...] Read more.
Some strains of Rhodococcus fascians exist only as epiphytes on the plant surface whereas others can become endophytic and cause various abnormalities including the release of multiple buds and reduced root growth. The abnormalities reflect the action of cytokinin. The strains that can become endophytic harbour a linear plasmid that carries cytokinin biosynthesis, activation and destruction genes. However, both epiphytic and endophytic forms can release cytokinin into culture, affect cytokinin metabolism within inoculated plants and enhance the expression of sugar and amino acid transporters and cell wall invertases, but only the endophytic form markedly affects the morphology of the plant. A unique methylated cytokinin, dimethylated N6-(∆2-isopentenyl)adenine (2-MeiP), operating in a high sugar environment, is the likely causative factor of the severe morphological abnormalities observed when plants are inoculated with R. fascians strains carrying the linear plasmid. Full article
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8 pages, 2763 KiB  
Brief Report
The Dynamics of Cytokinin Changes after Grafting of Vegetative Apices on Flowering Rapeseed Plants
by Danuše Tarkowská, Maria Filek, Jan Krekule, Jolanta Biesaga-Kościelniak, Izabela Marciñska, Marzena Popielarska-Konieczna and Miroslav Strnad
Plants 2019, 8(4), 78; https://doi.org/10.3390/plants8040078 - 28 Mar 2019
Cited by 5 | Viewed by 3242
Abstract
Despite numerous studies, the role of hormones in the induction of shoot apical meristem leading to reproductive development, especially regarding thermoperiodic plants, is still not fully understood. The key problem is separating the effects of the low temperature required for vernalization from those [...] Read more.
Despite numerous studies, the role of hormones in the induction of shoot apical meristem leading to reproductive development, especially regarding thermoperiodic plants, is still not fully understood. The key problem is separating the effects of the low temperature required for vernalization from those responsible for low temperature stress. An earlier experiment demonstrated the correlation between an increase of cytokinin level in the apical parts of winter rapeseed and the transition time into their reproductive phase during vernalization, i.e., low temperature treatment. From data obtained from the presented experiments, this study aims to contribute to the understanding the role of cytokinins in the induction of flowering based on the grafting of vegetative apical parts of winter rapeseed (scion) on the reproductive (stock) winter and spring genotypes. On the basis of analyses carried out using ultra-high-performance liquid chromatography coupled with tandem mass spectrometry in combination with microscopic observation of changes at the apical meristem, it was indicated that the increase in the amount of trans-zeatin and trans- and cis-zeatin-O-glucoside derivatives appeared in the early stages of apex floral differentiation. During further development, the content of all investigated cytokinins passed through the maximum level followed by their decrease. The final level in reproductive apices was found to be higher than that in vegetative ones. Full article
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