Timing Of Vegetative Phase Change Research Articles

Natural variation in CYCLIC NUCLEOTIDE-GATED ION CHANNEL 4 reveals a novel role of calcium signaling in vegetative phase change in Arabidopsis.

The timing of vegetative phase change (VPC) in plants is regulated by a temporal decline in the expression of miR156. Both exogenous cues and endogenous factors, such as temperature, light, sugar, nutrients, and epigenetic regulators, have been shown to affect VPC by altering miR156 expression. However, the genetic basis of natural variation in VPC remains largely unexplored. Here, we conducted a genome-wide association study on the variation of the timing of VPC in Arabidopsis. We identified CYCLIC NUCLEOTIDE-GATED ION CHANNEL 4 (CNGC4) as a significant locus associated with the diversity of VPC. Mutations in CNGC4 delayed VPC, accompanied by an increased expression level of miR156 and a corresponding decrease in SQUAMOSA PROMOTER BINDING-LIKE (SPL) gene expression. Furthermore, mutations in CNGC2 and CATION EXCHANGER 1/3 (CAX1/3) also led to a delay in VPC. Polymorphisms in the CNGC4 promoter contribute to the natural variation in CNGC4 expression and the diversity of VPC. Specifically, the early CNGC4 variant promotes VPC and enhances plant adaptation to local environments. In summary, our findings offer genetic insights into the natural variation in VPC in Arabidopsis, and reveal a previously unidentified role of calcium signaling in the regulation of VPC.

Vegetative phase change causes age-dependent changes in phenotypic plasticity.

Phenotypic plasticity allows organisms to optimize traits for their environment. As organisms age, they experience diverse environments that benefit from varying degrees of phenotypic plasticity. Developmental transitions can control these age-dependent changes in plasticity, and as such, the timing of these transitions can determine when plasticity changes in an organism. Here, we investigate how the transition from juvenile-to adult-vegetative development known as vegetative phase change (VPC) contributes to age-dependent changes in phenotypic plasticity and how the timing of this transition responds to environment using both natural accessions and mutant lines in the model plant Arabidopsis thaliana. We found that the adult phase of vegetative development has greater plasticity in leaf morphology than the juvenile phase and confirmed that this difference in plasticity is caused by VPC using mutant lines. Furthermore, we found that the timing of VPC, and therefore thetime when increased plasticity is acquired, varies significantly across genotypes and environments. The consistent age-dependent changes in plasticity caused by VPC suggest that VPC may be adaptive. This genetic and environmental variation in the timing of VPC indicates the potential for population-level adaptive evolution of VPC.

Identification of the Teopod1, Teopod2, and Early Phase Change genes in maize.

Teopod1 (Tp1), Teopod2 (Tp2), and Early phase change (Epc) have profound effects on the timing of vegetative phase change in maize. Gain-of-function mutations in Tp1 and Tp2 delay all known phase-specific vegetative traits, whereas loss-of-function mutations in Epc accelerate vegetative phase change and cause shoot abortion in some genetic backgrounds. Here, we show that Tp1 and Tp2 likely represent cis-acting mutations that cause the overexpression of Zma-miR156j and Zma-miR156h, respectively. Epc is the maize ortholog of HASTY, an Arabidopsis gene that stabilizes miRNAs and promotes their intercellular movement. Consistent with its pleiotropic phenotype and epistatic interaction with Tp1 and Tp2, epc reduces the levels of miR156 and several other miRNAs.

Divergent selection for timing of vegetative phase change

AbstractVegetative phase change is a key trait in plant development and marks the transition from juvenile to adult growth phases. In maize (Zea mays L.), juvenile plants and plants with a late phase change can be identified by the increased production of tillers, aerial roots, and distinctive epicuticular wax. Resistance to agronomically significant pathogens can also differ between juvenile and adult plants. Using last leaf with juvenile wax as the target of selection, the maize population Minnesota 11 underwent 16 cycles of divergent selection. The objectives of this research were to identify emergent trends for each trait and to determine the magnitude and direction of phenotypic changes over long‐term selection compared to the source population. Phenotypic data on plant architecture traits, ear traits, and common rust resistance were collected in 2020 and 2021 by concurrently growing plants from selection cycles representing both directions of selection. Last leaf with juvenile wax, the direct target of selection increased to leaf 17.8 in the late phase change population and decreased to leaf 5 in the early phase change population from leaf 9 in the source population. Late vegetative phase change was positively correlated with increased common rust infection and plant height, and negatively correlated with ear size traits. This study shows that the observed phenotypic changes follow patterns of genetic variation consistent with divergent selection, but with possible effects of inbreeding.

Reproductive competence is regulated independently of vegetative phase change in Arabidopsis thaliana

A long-standing question in plant biology is how the acquisition of reproductive competence is related to the juvenile-to-adult vegetative transition. We addressed this question by examining the expression pattern and mutant phenotypes of two families of miRNAs-miR156/miR157 and miR172-that operate in the same pathway and play important roles in these processes. The phenotype of mutants deficient for miR156/miR157, miR172, and all three miRNAs demonstrated that miR156/miR157 regulate the timing of vegetative phase change but have only a minor effect on reproductive competence, whereas miR172 has a minor role in vegetative phase change but has a major effect on reproductive competence. MIR172B is directly downstream of the miR156/SPL module, but temporal variation in the level of miR156 in the shoot apex and leaf-to-leaf variation in miR156 expression in young primordia was not associated with a change in the level of miR172 in these tissues. Additionally, although miR172 levels increase from leaf to leaf later in leaf development, this variation is largely insensitive to changes in the abundance of miR156. Our results indicate that the acquisition of reproductive competence in Arabidopsis is regulated by miR172 through a mechanism that is independent of the vegetative phase change pathway.

The genetic basis of natural variation in the timing of vegetative phase change in Arabidopsis thaliana.

The juvenile-to-adult transition in plants is known as vegetative phase change and is marked by changes in the expression of leaf traits in response to a decrease in the level of miR156 and miR157. To determine whether this is the only mechanism of vegetative phase change, we measured the appearance of phase-specific leaf traits in 70 natural accessions of Arabidopsis thaliana. We found that leaf shape was poorly correlated with abaxial trichome production (two adult traits), that variation in these traits was not necessarily correlated with the level of miR156, and that there was little to no correlation between the appearance of adult-specific vegetative traits and flowering time. We identified eight quantitative trait loci controlling phase-specific vegetative traits from a cross between the Columbia (Col-0) and Shakdara (Sha) accessions. Only one of these quantitative trait loci includes genes known to regulate vegetative phase change (MIR156A and TOE1), which were expressed at levels consistent with the precocious phenotype of Sha. Our results suggest that vegetative phase change is regulated both by the miR156/SPL module and by genes specific to different vegetative traits, and that natural variation in vegetative phase change can arise from either source.

ABI5 acts downstream of miR159 to delay vegetative phase change in Arabidopsis.

Vegetative development constitutes a critical phase in plant development, and it is regulated by an evolutionarily conserved miR156-SPL pathway. Previous studies have shown that miR159 acts to prevent the hyperactivation of miR156 to regulate the timing of vegetative phase change in Arabidopsis. However, whether miR159 integrates into the abscisic acid (ABA) signaling pathway to control vegetative phase change remains unexplored, since miR159 also plays an important regulatory role in ABA response. Here, we show that the expression of ABI5 (ABA INSENSITIVE5), a crucial regulator in the ABA signaling pathway, is significantly elevated in the loss-of-function mutant of miR159 (mir159ab). Loss of function in ABI5 (abi5) promotes juvenile-to-adult transition, whereas overexpression of ABI5 delays this transition under short-day conditions. Genetic analyses indicated that the effect of mir159ab on vegetative phase change is ABI5 dependent. Further analysis confirmed that MYB33, a major target of miR159, promotes the transcription of ABI5 by directly binding to its promoter. ABI5 functions upstream of miR156 to promote juvenile development by affecting the expression of genes in the miR156-SPL pathway. Therefore, our study uncovers a new role of ABI5 in vegetative development in plants, and implies a role of ABA signaling in vegetative development in Arabidopsis.

H2A.Z promotes the transcription of MIR156A and MIR156C in Arabidopsis by facilitating the deposition of H3K4me3.

Vegetative phase change in Arabidopsis thaliana is mediated by a decrease in the level of MIR156A and MIR156C, resulting in an increase in the expression of their targets, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes. Changes in chromatin structure are required for the downregulation of MIR156A and MIR156C, but whether chromatin structure contributes to their initial elevated expression is unknown. We found that mutations in components of the SWR1 complex (ARP6, SEF) and in genes encoding H2A.Z (HTA9 and HTA11) reduce the expression of MIR156A and MIR156C, and accelerate vegetative phase change, indicating that H2A.Z promotes juvenile vegetative identity. However, arp6 and sef did not accelerate the temporal decline in miR156, and the downregulation of MIR156A and MIR156C was not accompanied by significant change in the level of H2A.Z at these loci. We conclude that H2A.Z contributes to the high expression of MIR156A/MIR156C early in shoot development, but does not regulate the timing of vegetative phase change. Our results also suggest that H2A.Z promotes the expression of MIR156A/MIR156C by facilitating the deposition of H3K4me3, rather than by decreasing nucleosome occupancy.

A computational framework for mapping the timing of vegetative phase change.

Phase change plays a prominent role in determining the form of growth and development. Although considerable attention has been focused on identifying the regulatory control mechanisms of phase change, a detailed understanding of the genetic architecture of this phenomenon is still lacking. We address this issue by deriving a computational model. The model is founded on the framework of functional mapping aimed at characterizing the interplay between quantitative trait loci (QTLs) and development through biologically meaningful mathematical equations. A multiphasic growth equationwas implemented into functional mapping, which, via a series of hypothesis tests, allows the quantification of how QTLs regulate the timing and pattern of vegetative phase transition between independently regulated, temporally coordinated processes. The model was applied to analyze stem radial growth data of an interspecific hybrid family derived from two Populus species during the first 24yr of ontogeny. Several key QTLs related to phase change have been characterized, most of which were observed to be in the adjacent regions of candidate genes. The identification of phase transition QTLs, whose expression is regulated by endogenous and environmental signals, may enhance our understanding of the evolution of development in changing environments.

Large effect QTL explain natural phenotypic variation for the developmental timing of vegetative phase change in maize (Zea mays L.).

Natural variation for the timing of vegetative phase change in maize is controlled by several large effect loci, one corresponding to Glossy15 , a gene known for regulating juvenile tissue traits. Vegetative phase change is an intrinsic component of developmental programs in plants. Juvenile and adult vegetative tissues in grasses differ dramatically in their anatomical and biochemical composition affecting the utility of specific genotypes as animal feed and biofuel feedstock. The molecular network controlling the process of developmental transition is incompletely characterized. In this study, we used scoring for juvenile and adult epicuticular wax as an entry point to discover quantitative trait loci (QTL) controlling phenotypic variation for the developmental timing of juvenile to adult transition in maize. We scored the last leaf with juvenile wax on 25 recombinant inbred line families of the B73 reference Nested Association Mapping (NAM) population and the intermated B73×Mo17 (IBM) population across multiple seasons. A total of 13 unique QTL were identified through genome-wide association analysis across the NAM populations, three of which have large effects. A QTL located on chromosome nine had the most significant SNPs within Glossy15, a gene controlling expression of juvenile leaf traits. The second large effect QTL is located on chromosome two. The most significant SNP in this QTL is located adjacent to a homolog of the Arabidopsis transcription factor, enhanced downy mildew-2, which has been shown to promote the transition from juvenile to adult vegetative phase. Overall, these results show that several major QTL and potential candidate genes underlie the extensive natural variation for this developmental trait.

Genetic control of heterochrony in Eucalyptus globulus.

A change in the timing or rate of developmental events throughout ontogeny is referred to as heterochrony, and it is a major evolutionary process in plants and animals. We investigated the genetic basis for natural variation in the timing of vegetative phase change in the tree Eucalyptus globulus, which undergoes a dramatic change in vegetative morphology during the juvenile-to-adult transition. Quantitative trait loci analysis in an outcross F2 family derived from crosses between individuals from a coastal population of E. globulus with precocious vegetative phase change and individuals from populations in which vegetative phase change occurs several years later implicated the microRNA EglMIR156.5 as a potential contributor to this heterochronic difference. Additional evidence for the involvement of EglMIR156.5 was provided by its differential expression in trees with early and late phase change. Our findings suggest that changes in the expression of miR156 underlie natural variation in vegetative phase change in E. globulus, and may also explain interspecific differences in the timing of this developmental transition.

Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C.

Nutrients shape the growth, maturation, and aging of plants and animals. In plants, the juvenile to adult transition (vegetative phase change) is initiated by a decrease in miR156. In Arabidopsis, we found that exogenous sugar decreased the abundance of miR156, whereas reduced photosynthesis increased the level of this miRNA. This effect was correlated with a change in the timing of vegetative phase change, and was primarily attributable to a change in the expression of two genes, MIR156A and MIR156C, which were found to play dominant roles in this transition. The glucose-induced repression of miR156 was dependent on the signaling activity of HEXOKINASE1. We also show that the defoliation-induced increase in miR156 levels can be suppressed by exogenous glucose. These results provide a molecular link between nutrient availability and developmental timing in plants, and suggest that sugar is a component of the leaf signal that mediates vegetative phase change. DOI:http://dx.doi.org/10.7554/eLife.00260.001.

Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156

Vegetative phase change in Arabidopsis is regulated by miR156, a microRNA that promotes the expression of the juvenile phase and represses the expression of the adult phase. miR156 is expressed at a very high level early in shoot development and then decreases, leading to the onset of the adult phase. To determine the source of the factors that regulate vegetative phase change, we examined the effect of root and leaf ablation on the timing of this transition. Ablation of the root system or cotyledons had no effect on the timing of vegetative phase change, but ablation of leaf primordia delayed this transition in a miR156-dependent fashion. This treatment produced an increase in the overall abundance of miR156, which was attributable to an increase in the transcription of some, but not all, of the miR156 genes in Arabidopsis, and decreased the expression of SPL genes regulated by miR156. miR156 levels were also elevated by leaf ablation in Nicotiana benthamiana and in rejuvenating shoot apices of maize cultured in vitro. We conclude that vegetative phase change is initiated by a signal(s) produced by leaf primordia, which acts by repressing the transcription of specific members of the miR156 gene family.

Vegetative Phase Change Characteristics and Resistance to Common Rust of Corn Cultivars Developed in Different Eras

ABSTRACTSince 1930, maize (Zea mays L.) yields in the United States have increased more than fourfold. Previous studies examining maize cultivars grown during that period have documented changes in yield, leaf angle, tassel size, drought tolerance, and insect resistance, but none have examined changes in vegetative phase change or resistance to common rust (Puccinia sorghi Schwein.). Vegetative phase change has been shown to affect both disease and insect resistance, and common rust can reduce yields in maize especially east of the Mississippi River. Thirty‐six widely used northern Corn Belt cultivars spanning the years of pre‐1930 to 2006 were evaluated for phase change traits and rust resistance. Cultivars were divided into early and late maturity groups from different eras and planted at two locations with two planting dates per location for 2 yr. Timing of vegetative phase change has not changed linearly over the eras examined. There was, however, a significant linear increase in rust resistance over that time. In the early maturity group, percentage of leaf area infected by rust was found to decrease at a rate of 0.1% yr−1 Whole‐plant rust resistance in the late maturity group was found to increase at a rate of 0.05% yr−1.

Vegetative phase change among sweet corn (Zea mays L.) hybrids varying for reaction to common rust (Puccinia sorghi Schw.)

AbstractIn maize, timing of vegetative phase change has been implicated in the response to certain pests and environmental stresses. Common rust is the most serious disease of sweet corn in the north central United States. Sweet corn hybrids differing for resistance to common rust were evaluated for vegetative phase change traits. There were significant differences among hybrids for all vegetative phase change traits measured, as well as resistance to common rust. Certain hybrids displayed rapid transition (within two leaves) from juvenile to adult vegetation, while others displayed prolonged transition (within four leaves). There were no significant correlations between vegetative phase change traits and common rust severity among the commercial sweet corn hybrids evaluated in this experiment.

Quantitative Trait Locus Analysis of Stalk Strength in Four Maize Populations

Stalk lodging in maize (Zea mays L.) causes yield losses estimated to range from 5 to 20% annually worldwide. Selection for rind penetrometer resistance (RPR) has proven useful in enhancing germplasm for stalk strength, and therefore improving stalk lodging resistance. We conducted quantitative trait locus (QTL) analysis for RPR in four F 2.3 populations. The populations were constructed by means of combinations of MoSCSSS-High (selection for high RPR), MoSCSSS-Low (selection for low RPR), MoSQB-Low (selection for low stalk crushing strength), inbred line Mo47, and inbred line B73. Individuals in each population were genotyped for simple sequence repeat (SSR) or restriction fragment length polymorphism (RFLP) markers, and data were collected for RPR over multiple locations and replications. Means combined over environments were used as trait data for composite interval mapping by QTL Cartographer. Eight, 10, eight, and nine single-effect QTL and four, two, zero, and five epistatic interactions were detected for RPR in the four populations. Multilocus models, including the single-effect QTL and epistatic interactions, accounted for 33.4, 44.7, 48.4, and 58.7% of the total phenotypic variation. These data dearly indicate the complex nature of stalk strength. One chromosomal region contained a QTL from all four populations, while two QTL were in common among three of the four populations and five QTL were in common between two populations. Candidate genes that overlap QTL confidence intervals include those involved in lignin synthesis, the phenylpropanoid pathway, and the timing of vegetative phase change.

Quantitative genetic evidence that the timing of vegetative phase change in Eucalyptus globulus ssp. globulus is an adaptive trait

Quantitative genetic analysis of six field trials suggests a complex pattern of adaptive significance for the timing of the abrupt change in leaf form in Eucalyptus globulus Labill. spp. globulus. Data from one small trial demonstrated a genetic basis to a steep local cline in habit, in the size of plants flowering and in the height of the change in foliage type. Thus, slow growth, early phase change and precocious flowering appear to be maintained in exposed coastal environments by current selection. This contrasts with results from five large trials that contained open-pollinated progeny from across the whole geographic range of this taxon. On this broad scale, early phase change appears to promote growth, a fitness surrogate, in two trials but not the others, implying differential selection for the timing of phase change. In these cases, early phase change may have been favoured in warm, wet environments by reducing damage by leaf fungi. There was marked genetic variation in the timing of vegetative phase change among broad regions, consistent with either adaptation to broad-scale environmental variation or historical differentiation.

Strong, independent, quantitative genetic control of the timing of vegetative phase change and first flowering in eucalyptus globulus ssp. globulus (Tasmanian blue gum)

Analyses of large open-pollinated and controlled-cross field trials of Eucalyptus globulus ssp. globulus show quantitative genetic independence of the times of first flowering and the abrupt change in leaf form. The onset of each of these critical developmental events is under moderate to strong additive genetic control in this taxon, with individual narrow-sense heritabilities of 0.4-0.6 and 0. 2-0.9, respectively, and little nonadditive genetic control. This strong additive genetic control and the independence of these processes provide the genetic environment for rapid heterochronic microevolution.

Strong, independent, quantitative genetic control of the timing of vegetative phase change and first flowering in Eucalyptus globulus ssp. globulus (Tasmanian Blue Gum)

Strong, independent, quantitative genetic control of the timing of vegetative phase change and first flowering in Eucalyptus globulus ssp. globulus (Tasmanian Blue Gum)

Developmental Changes Associated with Divergent Selection for Rind Penetrometer Resistance in the MoSCSSS Maize Synthetic

Rind penetrometer resistance (RPR) has been used to select indirectly for stalk lodging resistance in maize (Zea mays L.). Breeding for stalk lodging resistance would be facilitated by a better understanding of developmental mechanisms affecting RPR. Vegetative development can be divided into juvenile‐vegetative and adult‐vegetative phases. Vegetative phase change occurs when juvenile‐vegetative traits are replaced by adult‐vegetative traits. The objective of this study was to determine indirect responses in the timing of vegetative phase change and other developmental traits in nine cycles of S0 phenotypic divergent selection for RPR in Missouri Second Cycle Stiff Stalk Synthetic (MoSCSSS). In the high direction of selection, vegetative phase change occurred at lower nodes while ear leaf number and total leaf number decreased. In the low direction of selection, vegetative phase change was delayed to higher nodes while ear leaf number and total leaf number increased. In both directions of selection, plant height was reduced and flowering occurred earlier. The timing of vegetative phase change may be a factor in determining the level of RPR and stalk lodging resistance. Alternatively, modifiers may exist in MoSCSSS that coordinately regulate vegetative phase change with traits, such as ear leaf number, that are directly affected by selection for RPR.