Summary
The plasticity of growth and development in response to environmental changes is one of the essential aspects of plant behavior. Cytokinins play an important role as signaling molecules in ...the long‐distance communication between organs in systemic growth regulation in response to nitrogen. The spatial distribution of the expression sites of cytokinin biosynthesis genes leads to structural differences in the molecular species transported through the xylem and phloem, giving root‐borne trans‐hydroxylated cytokinins, namely trans‐zeatin (tZ) type, a specialized efficacy in regulating shoot growth. Furthermore, root‐to‐shoot translocation via the xylem, tZ, and its precursor, the tZ riboside, controls different sets of shoot growth traits to fine‐tune shoot growth in response to nitrogen availability. In addition to nitrogen, photosynthetically generated sugars positively regulate de novo cytokinin biosynthesis in the roots, and contribute to plant growth under elevated CO2 conditions. In shoot‐to‐root signaling, cytokinins also play a role in the regulation of nutrient acquisition and root system growth in cooperation with other types of signaling molecules, such as C‐TERMINALLY ENCODED PEPTIDE DOWNSTREAMs. As cytokinin is a key regulator for the maintenance of shoot apical meristem, deepening our understanding of the regulatory mechanisms of cytokinin biosynthesis and transport in response to nitrogen is important not only for basic comprehension of plant growth, but also to ensure the stability of agricultural production.
Significance Statement
This review article provides an overview of recent advances in the study of nitrogen‐dependent biosynthesis and transport of cytokinin, a growth‐promoting phytohormone, especially focusing on the role as systemic nutritional signaling. Quantitative and qualitative regulation of cytokinin action fine‐tunes plant growth manner in response to nitrogen availability.
Cytokinins (CKs) play a crucial role in various phases of plant growth and development, but the basic molecular mechanisms of their biosynthesis and signal transduction only recently became clear. ...The progress was achieved by identifying a series of key genes encoding enzymes and proteins controlling critical steps in biosynthesis, translocation, and signaling. Basic schemes for CK homeostasis and root/shoot communication at the whole-plant level can now be devised. This review summarizes recent findings on the relationship between CK structural variation and activity, distinct features in CK biosynthesis between higher plants and Agrobacterium infected plants, CK translocation at whole-plant and cellular levels, and CKs as signaling molecules for nutrient status via root-shoot communication.
Nitrogen is the mineral nutrient that often limits plant growth and development. In response to changes in nitrogen supply, plants display elaborate responses at both physiological and morphological ...levels to adjust their growth and development. Because higher plants consist of multiple organs with different functions and nutritional requirements, they rely on local and long-distance signalling pathways to coordinate the responses at the whole-plant level. Phytohormones have been considered as signalling substances of such pathways. Amongst phytohormones, abscisic acid, auxin, and cytokinins have been closely linked to nitrogen signalling. Recent evidence has provided some insights into how nitrogen and the phytohormone signals are integrated to bring about changes in physiology and morphology. In this review, the evidence is summarized, mostly focusing on examples related to nitrogen acquisition.
Abstract
Plants use nitrate, ammonium, and organic nitrogen in the soil as nitrogen sources. Since the elevated CO
2
environment predicted for the near future will reduce nitrate utilization by C
3
...species, ammonium is attracting great interest. However, abundant ammonium nutrition impairs growth, i.e., ammonium toxicity, the primary cause of which remains to be determined. Here, we show that ammonium assimilation by GLUTAMINE SYNTHETASE 2 (GLN2) localized in the plastid rather than ammonium accumulation is a primary cause for toxicity, which challenges the textbook knowledge. With exposure to toxic levels of ammonium, the shoot GLN2 reaction produced an abundance of protons within cells, thereby elevating shoot acidity and stimulating expression of acidic stress-responsive genes. Application of an alkaline ammonia solution to the ammonium medium efficiently alleviated the ammonium toxicity with a concomitant reduction in shoot acidity. Consequently, we conclude that a primary cause of ammonium toxicity is acidic stress.
The notion that plants use specialized metabolism to protect against environmental stresses needs to be experimentally proven by addressing the question of whether stress tolerance by specialized ...metabolism is directly due to metabolites such as flavonoids. We report that flavonoids with radical scavenging activity mitigate against oxidative and drought stress in Arabidopsis thaliana. Metabolome and transcriptome profiling and experiments with oxidative and drought stress in wild‐type, single overexpressors of MYB12/PFG1 (PRODUCTION OF FLAVONOL GLYCOSIDES1) or MYB75/PAP1 (PRODUCTION OF ANTHOCYANIN PIGMENT1), double overexpressors of MYB12 and PAP1, transparent testa4 (tt4) as a flavonoid‐deficient mutant, and flavonoid‐deficient MYB12 or PAP1 overexpressing lines (obtained by crossing tt4 and the individual MYB overexpressor) demonstrated that flavonoid overaccumulation was key to enhanced tolerance to such stresses. Antioxidative activity assays using 2,2‐diphenyl‐1‐picrylhydrazyl, methyl viologen, and 3,3′‐diaminobenzidine clearly showed that anthocyanin overaccumulation with strong in vitro antioxidative activity mitigated the accumulation of reactive oxygen species in vivo under oxidative and drought stress. These data confirm the usefulness of flavonoids for enhancing both biotic and abiotic stress tolerance in crops.
Cytokinins (CKs), a class of plant hormones, are central regulators of plant growth and development. Based on numerous physiological and genetic studies, the quantitative regulation of cytokinin ...levels is the major mechanism regulating cytokinin action in diverse developmental processes. Here, we identified a different mechanism with which the physiological function of CK is modulated through side-chain modification (trans-hydroxylation). The trans-hydroxylation that forms trans-zeatin (tZ)-type CK from N6-(Δ2-isopentenyl)adenine (iP)-type CK is catalyzed by the cytochrome P450 enzymes CYP735A1 and CYP735A2 in Arabidopsis. Deficiency in trans-hydroxylation activity results in dramatic retardation of shoot growth without affecting total CK quantity, while augmentation of the activity enhances shoot growth. Application of exogenous tZ but not iP recovers the wild-type phenotype in the mutants, indicating that trans-hydroxylation modifies the physiological function of CK. We propose that the control of cytokinin function by side-chain modification is crucial for shoot growth regulation in plants.
•The trans-hydroxylation of CK is catalyzed by CYP735A1/A2 in Arabidopsis•trans-hydroxylated CKs are required for shoot growth but dispensable for root growth•trans-hydroxylation of CKs affects their efficacy but not total CK levels
Cytokinins (CKs) are phytohormones that control diverse processes of plant growth and development. Kiba et al. find that side-chain modification (trans-hydroxylation) of CK molecular structure regulates the efficacy of CK action independent of any effects on CK levels, and trans-hydroxylated CK is required for shoot growth but not root growth.
Abstract
Carbon availability is a major regulatory factor in plant growth and development. Cytokinins, plant hormones that play important roles in various aspects of growth and development, have been ...implicated in the carbon-dependent regulation of plant growth; however, the details of their involvement remain to be elucidated. Here, we report that sugar-induced cytokinin biosynthesis plays a role in growth enhancement under elevated CO
2
in
Arabidopsis thaliana
. Growing Arabidopsis seedlings under elevated CO
2
resulted in an accumulation of cytokinin precursors that preceded growth enhancement. In roots, elevated CO
2
induced two genes involved in
de novo
cytokinin biosynthesis: an adenosine phosphate-isopentenyltransferase gene,
AtIPT3
, and a cytochrome P450 monooxygenase gene,
CYP735A2
. The expression of these genes was inhibited by a photosynthesis inhibitor, DCMU, under elevated CO
2
, and was enhanced by sugar supplements, indicating that photosynthetically generated sugars are responsible for the induction. Consistently, cytokinin precursor accumulation was enhanced by sugar supplements. Cytokinin biosynthetic mutants were impaired in growth enhancement under elevated CO
2
, demonstrating the involvement of
de novo
cytokinin biosynthesis for a robust growth response. We propose that plants employ a system to regulate growth in response to elevated CO
2
in which photosynthetically generated sugars induce
de novo
cytokinin biosynthesis for growth regulation.
Stomata play an important role in preinvasive defense responses by limiting pathogen entry into leaves. Although the stress hormones salicylic acid (SA) and abscisic acid (ABA) are known to regulate ...stomatal immunity, the role of growth promoting hormones is far from understood. Here, we show that in Arabidopsis thaliana, cytokinins (CKs) function in stomatal defense responses. The cytokinin receptor HISTIDINE KINASE3 (AHK3) and RESPONSE REGULATOR2 (ARR2) promote stomatal closure triggered by pathogen-associated molecular pattern (PAMP) and resistance to Pseudomonas syringae pv tomato bacteria. Importantly, the cytokinin trans-zeatin induces stomatal closure and accumulation of reactive oxygen species (ROS) in guard cells through AHK3 and ARR2 in an SA-dependent and ABA-independent manner. Using pharmacological and reverse genetics approaches, we found that CK-mediated stomatal responses involve the apoplastic peroxidases PRX4, PRX33, PRX34, and PRX71, but not the NADPH oxidases RBOHD and RBOHF. Moreover, ARR2 directly activates the expression of PRX33 and PRX34, which are required for SA- and PAMP-triggered ROS production. Thus, the CK signaling pathway regulates ROS homeostasis in guard cells, which leads to enhanced stomatal immunity and plant resistance to bacteria.
Nitrate is a nutrient signal that triggers complex regulation of transcriptional networks to modulate nutrient-dependent growth and development in plants. This includes time- and nitrate ...concentration-dependent regulation of nitrate-related gene expression. However, the underlying mechanisms remain poorly understood. Here we identify NIGT1 transcriptional repressors as negative regulators of the Arabidopsis NRT2.1 nitrate transporter gene, and show antagonistic regulation by NLP primary transcription factors for nitrate signalling and the NLP-NIGT1 transcriptional cascade-mediated repression. This antagonistic regulation provides a resolution to the complexity of nitrate-induced transcriptional regulations. Genome-wide analysis reveals that this mechanism is applicable to NRT2.1 and other genes involved in nitrate assimilation, hormone biosynthesis and transcription. Furthermore, the PHR1 master regulator of the phosphorus-starvation response also directly promotes expression of NIGT1 family genes, leading to reductions in nitrate uptake. NIGT1 repressors thus act in two transcriptional cascades, forming a direct link between phosphorus and nitrogen nutritional regulation.
Wild and weedy relatives of domesticated crops harbor genetic variants that can advance agricultural biotechnology. Here we provide a genome resource for the wild plant green millet (Setaria ...viridis), a model species for studies of C
grasses, and use the resource to probe domestication genes in the close crop relative foxtail millet (Setaria italica). We produced a platinum-quality genome assembly of S. viridis and de novo assemblies for 598 wild accessions and exploited these assemblies to identify loci underlying three traits: response to climate, a 'loss of shattering' trait that permits mechanical harvest and leaf angle, a predictor of yield in many grass crops. With CRISPR-Cas9 genome editing, we validated Less Shattering1 (SvLes1) as a gene whose product controls seed shattering. In S. italica, this gene was rendered nonfunctional by a retrotransposon insertion in the domesticated loss-of-shattering allele SiLes1-TE (transposable element). This resource will enhance the utility of S. viridis for dissection of complex traits and biotechnological improvement of panicoid crops.
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