A role of the plant hormone cytokinin in regulating the development and activity of chloroplasts was described soon after its discovery as a plant growth regulator more than 50 years ago. Its ...promoting action on chloroplast ultrastructure and chlorophyll synthesis has been reported repeatedly, especially during etioplast-to-chloroplast transition. Recently, a protective role of the hormone for the photosynthetic apparatus during high light stress was shown. Details about the molecular mechanisms of cytokinin action on plastids are accumulating from genetic and transcriptomic studies. The cytokinin receptors AHK2 and AHK3 are mainly responsible for the transduction of the cytokinin signal to B-type response regulators, in particular ARR1, ARR10, and ARR12, which are transcription factors of the two-component system mediating cytokinin functions. Additional transcription factors linking cytokinin and chloroplast development include CGA1, GNC, HY5, GLK2, and CRF2. In this review, we summarize early and more recent findings of the long-known relationship between the hormone and the organelle and describe crosstalk between cytokinin, light, and other hormones during chloroplast development.
The phytohormone cytokinin was originally discovered as a regulator of cell division. Later, it was described to be involved in regulating numerous processes in plant growth and development including ...meristem activity, tissue patterning, and organ size. More recently, diverse functions for cytokinin in the response to abiotic and biotic stresses have been reported. Cytokinin is required for the defence against high light stress and to protect plants from a novel type of abiotic stress caused by an altered photoperiod. Additionally, cytokinin has a role in the response to temperature, drought, osmotic, salt, and nutrient stress. Similarly, the full response to certain plant pathogens and herbivores requires a functional cytokinin signalling pathway. Conversely, different types of stress impact cytokinin homeostasis. The diverse functions of cytokinin in responses to stress and crosstalk with other hormones are described. Its emerging roles as a priming agent and as a regulator of growth‐defence trade‐offs are discussed.
This review describes the numerous functions of cytokinin in the defence against abiotic and biotic stresses, highlighting signalling pathways responding to light stress, drought, or pathogen attack. The role of cytokinin in priming and regulating growth‐defence trade‐off is addressed as well.
Light is important for plants as an energy source and a developmental signal, but it can also cause stress to plants and modulates responses to stress. Excess and fluctuating light result in ...photoinhibition and reactive oxygen species (ROS) accumulation around photosystems II and I, respectively. Ultraviolet light causes photodamage to DNA and a prolongation of the light period initiates the photoperiod stress syndrome. Changes in light quality and quantity, as well as in light duration are also key factors impacting the outcome of diverse abiotic and biotic stresses. Short day or shady environments enhance thermotolerance and increase cold acclimation. Similarly, shade conditions improve drought stress tolerance in plants. Additionally, the light environment affects the plants' responses to biotic intruders, such as pathogens or insect herbivores, often reducing growth‐defence trade‐offs. Understanding how plants use light information to modulate stress responses will support breeding strategies to enhance crop stress resilience. This review summarizes the effect of light as a stressor and the impact of the light environment on abiotic and biotic stress responses. There is a special focus on the role of the different light receptors and the crosstalk between light signalling and stress response pathways.
Light can be stressful for plants and the light environment (quality, quantity and duration of illumination) influences the responses of plants to biotic and abiotic stresses through diverse connections between the light and stress signaling pathways.
Because stress experiences are often recurrent plants have developed strategies to remember a first so-called priming stress to eventually respond more effectively to a second triggering stress. ...Here, we have studied the impact of discontinuous or sustained cold stress (4 °C) on in vitro grown Arabidopsis thaliana seedlings of different age and their ability to get primed and respond differently to a later triggering stress. Cold treatment of 7-d-old seedlings induced the expression of cold response genes but did not cause a significantly enhanced freezing resistance. The competence to increase the freezing resistance in response to cold was associated with the formation of true leaves. Discontinuous exposure to cold only during the night led to a stepwise modest increase in freezing tolerance provided that the intermittent phase at ambient temperature was less than 32 h. Seedlings exposed to sustained cold treatment developed a higher freezing tolerance which was further increased in response to a triggering stress during three days after the priming treatment had ended indicating cold memory. Interestingly, in all scenarios the primed state was lost as soon as the freezing tolerance had reached the level of naïve plants indicating that an effective memory was associated with an altered physiological state. Known mutants of the cold stress response (cbfs, erf105) and heat stress memory (fgt1) did not show an altered behaviour indicating that their roles do not extend to memory of cold stress in Arabidopsis seedlings.
Cytokinin action in plant development Werner, Tomáš; Schmülling, Thomas
Current opinion in plant biology,
10/2009, Volume:
12, Issue:
5
Journal Article
Peer reviewed
Cytokinin regulates many important aspects of plant development in aerial and subterranean organs. The hormone is part of an intrinsic genetic network controlling organ development and growth in ...these two distinct environments that plants have to cope with. Cytokinin also mediates the responses to variable extrinsic factors, such as light conditions in the shoot and availability of nutrients and water in the root, and has a role in the response to biotic and abiotic stress. Together, these activities contribute to the fine-tuning of quantitative growth regulation in plants. We review recent progress in understanding the cytokinin system and its links to the regulatory pathways that respond to internal and external signals.
Abstract
During vegetative growth plants pass from a juvenile to an adult phase causing changes in shoot morphology. This vegetative phase change is primarily regulated by the opposite actions of two ...microRNAs, the inhibitory miR156 and the promoting miR172 as well as their respective target genes, constituting the age pathway. Here we show that the phytohormone cytokinin promotes the juvenile-to-adult phase transition through regulating components of the age pathway. Reduction of cytokinin signalling substantially delayed the transition to the adult stage.
t
Z-type cytokinin was particularly important as compared to iP- and the inactive
c
Z-type cytokinin, and root-derived
t
Z influenced the phase transition significantly. Genetic and transcriptional analyses indicated the requirement of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors and miR172 for cytokinin activity. Two miR172 targets,
TARGET OF EAT1
(
TOE1
) and
TOE2
encoding transcriptional repressors were necessary and sufficient to mediate the influence of cytokinin on vegetative phase change. This cytokinin pathway regulating plant aging adds to the complexity of the regulatory network controlling the juvenile-to-adult phase transition and links cytokinin to miRNA action.
Understanding the response to cold temperature stress is relevant for both basic biology and application. Here we report on ERF105, which is a novel cold‐regulated transcription factor gene of ...Arabidopsis that makes a significant contribution to freezing tolerance and cold acclimation. The expression of cold‐responsive genes in erf105 mutants suggests that its action is linked to the CBF regulon mediating cold responses.
Low temperature is an environmental factor that adversely affects plant growth and development and limits the geographical distribution of species; it impacts also the agronomical performance of crop plants. Therefore, understanding the response to cold‐temperature stress is relevant for both basic biology and application. In this work, we report the characterization of an APETALA2 (AP2)/ERF domain‐containing transcription factor gene of Arabidopsis, ERF105. ERF105 expression is induced by cold, and we show that the gene is functionally important for the cold stress response. Its effect on freezing tolerance is comparable or even higher than the one of components of the well‐studied CBF regulon, and the expression behaviour of cold‐responsive genes indicates that ERF105 may act upstream of the well‐known CBF regulon. Taken together, we think that this is a novel and relevant contribution for our understanding of the response of plants to cold stress.
Recently, a novel type of abiotic stress caused by a prolongation of the light period—coined photoperiod stress—has been described in Arabidopsis. During the night after the prolongation of the light ...period, stress and cell death marker genes are induced. The next day, strongly stressed plants display a reduced photosynthetic efficiency and leaf cells eventually enter programmed cell death. The phytohormone cytokinin (CK) acts as a negative regulator of this photoperiod stress syndrome. In this study, we show that Arabidopsis wild‐type plants increase the CK concentration in response to photoperiod stress. Analysis of cytokinin synthesis and transport mutants revealed that root‐derived trans‐zeatin (tZ)‐type CKs protect against photoperiod stress. The CK signalling proteins ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 2 (AHP2), AHP3 and AHP5 and transcription factors ARABIDOPSIS RESPONSE REGULATOR 2 (ARR2), ARR10 and ARR12 are required for the protective activity of CK. Analysis of higher order B‐type arr mutants suggested that a complex regulatory circuit exists in which the loss of ARR10 or ARR12 can rescue the arr2 phenotype. Together the results revealed the role of root‐derived CK acting in the shoot through the two‐component signalling system to protect from the negative consequences of strong photoperiod stress.
A prolongation of the light period induces in Arabidopsis photoperiod stress accompanied by an increase in cytokinin concentration. It is shown that root‐derived trans‐zeatin‐type cytokinin is essential to cope with photoperiod stress by signaling through the two‐component signaling proteins AHP2,3,5 and ARR2,10,12.
We used loss-of-function mutants to study three Arabidopsis thaliana sensor histidine kinases, AHK2, AHK3, and CRE1/AHK4, known to be cytokinin receptors. Mutant seeds had more rapid germination, ...reduced requirement for light, and decreased far-red light sensitivity, unraveling cytokinin functions in seed germination control. Triple mutant seeds were more than twice as large as wild-type seeds. Genetic analysis indicated a cytokinin-dependent endospermal and/or maternal control of embryo size. Unchanged red light sensitivity of mutant hypocotyl elongation suggests that previously reported modulation of red light signaling by A-type response regulators may not depend on cytokinin. Combined loss of AHK2 and AHK3 led to the most prominent changes during vegetative development. Leaves of ahk2 ahk3 mutants formed fewer cells, had reduced chlorophyll content, and lacked the cytokinin-dependent inhibition of dark-induced chlorophyll loss, indicating a prominent role of AHK2 and, particularly, AHK3 in the control of leaf development. ahk2 ahk3 double mutants developed a strongly enhanced root system through faster growth of the primary root and, more importantly, increased branching. This result supports a negative regulatory role for cytokinin in root growth regulation. Increased cytokinin content of receptor mutants indicates a homeostatic control of steady state cytokinin levels through signaling. Together, the analyses reveal partially redundant functions of the cytokinin receptors and prominent roles for the AHK2/AHK3 receptor combination in quantitative control of organ growth in plants, with opposite regulatory functions in roots and shoots.
Degradation of the plant hormone cytokinin is catalyzed by cytokinin oxidase/dehydrogenase (CKX) enzymes. The Arabidopsis thaliana genome encodes seven CKX proteins which differ in subcellular ...localization and substrate specificity. Here we analyze the CKX7 gene, which to the best of our knowledge has not yet been studied. pCKX7:GUS expression was detected in the vasculature, the transmitting tissue and the mature embryo sac. A CKX7–GFP fusion protein localized to the cytosol, which is unique among all CKX family members. 35S:CKX7‐expressing plants developed short, early terminating primary roots with smaller apical meristems, contrasting with plants overexpressing other CKX genes. The vascular bundles of 35S:CKX7 primary roots contained only protoxylem elements, thus resembling the wol mutant of the CRE1/AHK4 receptor gene. We show that CRE1/AHK4 activity is required to establish the CKX7 overexpression phenotype. Several cytokinin metabolites, in particular cis‐zeatin (cZ) and N‐glucoside cytokinins, were depleted stronger in 35S:CKX7 plants compared with plants overexpressing other CKX genes. Interestingly, enhanced protoxylem formation together with reduced primary root growth was also found in the cZ‐deficient tRNA isopentenyltransferase mutant ipt2,9. However, different cytokinins were similarly efficient in suppressing 35S:CKX7 and ipt2,9 vascular phenotypes. Therefore, we hypothesize that the pool of cytosolic cytokinins is particularly relevant in the root procambium where it mediates the differentiation of vascular tissues through CRE1/AHK4. Taken together, the distinct consequences of CKX7 overexpression indicate that the cellular compartmentalization of cytokinin degradation and substrate preference of CKX isoforms are relevant parameters that define the activities of the hormone.
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