Molecular control of seasonal flowering in rice,arabidopsis and temperate cereals

Background

Rice (Oryza sativa) and Arabidopsis thaliana have been widely used as model systems to understand how plants control flowering time in response to photoperiod and cold exposure. Extensive research has resulted in the isolation of several regulatory genes involved in flowering and for them to be organized into a molecular network responsive to environmental cues. When plants are exposed to favourable conditions, the network activates expression of florigenic proteins that are transported to the shoot apical meristem where they drive developmental reprogramming of a population of meristematic cells. Several regulatory factors are evolutionarily conserved between rice and arabidopsis. However, other pathways have evolved independently and confer specific characteristics to flowering responses.

Scope

This review summarizes recent knowledge on the molecular mechanisms regulating daylength perception and flowering time control in arabidopsis and rice. Similarities and differences are discussed between the regulatory networks of the two species and they are compared with the regulatory networks of temperate cereals, which are evolutionarily more similar to rice but have evolved in regions where exposure to low temperatures is crucial to confer competence to flower. Finally, the role of flowering time genes in expansion of rice cultivation to Northern latitudes is discussed.

Conclusions

Understanding the mechanisms involved in photoperiodic flowering and comparing the regulatory networks of dicots and monocots has revealed how plants respond to environmental cues and adapt to seasonal changes. The molecular architecture of such regulation shows striking similarities across diverse species. However, integration of specific pathways on a basal scheme is essential for adaptation to different environments. Artificial manipulation of flowering time by means of natural genetic resources is essential for expanding the cultivation of cereals across different environments.     

Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity

The control of flowering is central to reproductive success in plants, and has a major impact on grain yield in crop species. The global importance of temperate cereal crops such as wheat and barley has meant emphasis has long been placed on understanding the genetics of flowering in order to enhance yield. Leads gained from the dissection of the molecular genetics of model species have combined with comparative genetic approaches, recently resulting in the isolation of the first flowering time genes in wheat and barley. This paper reviews the genetics and genes involved in cereal flowering pathways and the current understanding of how two of the principal genes, Vrn and Ppd, have been involved in domestication and adaptation to local environments, and the implications for future breeding programmes are discussed.     

The genetic basis of flowering responses to seasonal cues

Plants respond to the changing seasons to initiate developmental programmes precisely at particular times of year. Flowering is the best characterized of these seasonal responses, and in temperate climates it often occurs in spring. Genetic approaches in Arabidopsis thaliana have shown how the underlying responses to changes in day length (photoperiod) or winter temperature (vernalization) are conferred and how these converge to create a robust seasonal response. Recent advances in plant genome analysis have demonstrated the diversity in these regulatory systems in many plant species, including several crops and perennials, such as poplar trees. Here, we report progress in defining the diverse genetic mechanisms that enable plants to recognize winter, spring and autumn to initiate flower development.     

Inheritance of time to flowering in chickpea in a short-season temperate environment

Time to flowering is central in determining the adaptation and productivity of chickpea in short-season temperate environments. We studied the genetic control of this trait in three crosses, 272-2 x CDC Anna, 298T-9 x CDC Anna, and 298T-9 x CDC Frontier. From each cross, 180 F2 plants and parents were evaluated for time to flowering under greenhouse conditions. In summer 2004, multiple generations including P1, F1, P2, F2, and F2:3 (also called MG5) were evaluated for time to flowering under field conditions. The data on time to flowering in the F(2) populations were continuous in distribution but deviated from normal distribution. The F2:3 families derived from this showed a bimodal distribution for time to flowering, a typical case of major-gene inheritance model with duplicate recessive epistasis. A joint segregation analysis of MG5 also revealed that time to flowering in chickpea was controlled by two major genes along with other polygenes. Late flowering was dominant over early flowering for both major genes with digenic interaction between them, mainly an additive x additive type. This information can be used to formulate the most efficient breeding strategy for improvement of time to flowering in chickpea in short-season temperate environments.     

The molecular basis of vernalization-induced flowering in cereals

Genetic analyses have identified three genes that control the vernalization requirement in wheat and barley; VRN1, VRN2 and FT (VRN3). These genes have now been isolated and shown to regulate not only the vernalization response but also the promotion of flowering by long days. VRN1 is induced by vernalization and accelerates the transition to reproductive development at the shoot apex. FT is induced by long days and further accelerates reproductive apex development. VRN2, a floral repressor, integrates vernalization and day-length responses by repressing FT until plants are vernalized. A comparison of flowering time pathways in cereals and Arabidopsis shows that the vernalization response is controlled by different MADS box genes, but integration of vernalization and long-day responses occurs through similar mechanisms.     

Climate change and the optimal flowering time of annual plants in seasonal environments

Long‐term phenology monitoring has documented numerous examples of changing flowering dates during the last century. A pivotal question is whether these phenological responses are adaptive or not under directionally changing climatic conditions. We use a classic dynamic growth model for annual plants, based on optimal control theory, to find the fitness‐maximizing flowering time, defined as the switching time from vegetative to reproductive growth. In a typical scenario of global warming, with advanced growing season and increased productivity, optimal flowering time advances less than the start of the growing season. Interestingly, increased temporal spread in production over the season may either advance or delay the optimal flowering time depending on overall productivity or season length. We identify situations where large phenological changes are necessary for flowering time to remain optimal. Such changes also indicate changed selection pressures. In other situations, the model predicts advanced phenology on a calendar scale, but no selection for early flowering in relation to the start of the season. We also show that the optimum is more sensitive to increased productivity when productivity is low than when productivity is high. All our results are derived using a general, graphical method to calculate the optimal flowering time applicable for a large range of shapes of the seasonal production curve. The model can thus explain apparent maladaptation in phenological responses in a multitude of scenarios of climate change. We conclude that taking energy allocation trade‐offs and appropriate time scales into account is critical when interpreting phenological patterns.     

An augmented Arabidopsis phenology model reveals seasonal temperature control of flowering time

? In this study, we used a combination of theoretical (models) and experimental (field data) approaches to investigate the interaction between light and temperature signalling in the control of Arabidopsis flowering. ? We utilised our recently published phenology model that describes the flowering time of Arabidopsis grown under a range of field conditions. We first examined the ability of the model to predict the flowering time of field plantings at different sites and seasons in light of the specific meteorological conditions that pertained. ? Our analysis suggested that the synchrony of temperature and light cycles is important in promoting floral initiation. New features were incorporated into the model that improved its predictive accuracy across seasons. Using both laboratory and field data, our study has revealed an important seasonal effect of night temperatures on flowering time. Further model adjustments to describe phytochrome (phy) mutants supported our findings and implicated phyB in the temporal gating of temperature-induced flowering. ? Our study suggests that different molecular pathways interact and predominate in natural environments that change seasonally. Temperature effects are mediated largely during the photoperiod during spring/summer (long days) but, as days shorten in the autumn, night temperatures become increasingly important.     

B chromosomes in hybrids of temperate cereals and grasses

B chromosomes are considered to be genetically inert, yet often have pronounced and surprising effects upon the A chromosome behaviour at meiosis in inter-generic and inter-specific hybrids. We review here our current knowledge of these effects in a number of different hybrids of the temperate cereals and grasses. Through hybridisation, many effects comparable to the pairing control system of wheat are uncovered, together with complex interactions of B chromosomes with hybrid host genotypes. We discuss the genetic and physical basis of the effects and try to make sense of them in terms of what we know about the origin and evolution of B chromosomes in plants.     

Induction of flowering by seasonal changes in photoperiod

In many plants, major developmental transitions such as the initiation of flowering are synchronized to the changing seasons. Day length provides one of the environmental cues used to achieve this. We describe the molecular mechanisms that measure day length and control flowering in Arabidopsis. Also, we compare these mechanisms with those that control flowering time in rice. This comparison suggests that components of the Arabidopsis regulatory network are conserved in other species, but that their regulation can be altered to generate different phenotypic responses.     

Effects of shift in flowering time on the reproductive output of Xanthium canadense in a seasonal environment

We studied the effects of a change in flowering date on the reproductive output of a short-day annual plant, Xanthium canadense. The flowering date was changed by photoperiodic manipulation to 1 month earlier or later than the natural flowering date. Plants with the natural flowering date attained the highest reproductive output. For those flowering 1 month earlier or later, the reproductive output was decreased by 42% or 23%, respectively. The reproductive output was analyzed as the product of the biomass production during the reproductive period and its allocation to the reproductive organs. Although delay in flowering increased biomass production, it decreased its fractional allocation to the reproductive organs. The highest reproductive output in the natural flowering plants resulted from a compromise between these two effects of flowering. Plants flowering earlier had higher translocation rates to the reproductive organs and accelerated plant senescence. Later flowering caused a reduction in biomass translocation to the reproductive organs and thus extended the reproductive period. These experimental results are discussed in relation to the cost of reproduction and the optimal time for flowering that maximizes the final reproductive output. It is suggested that the natural flowering time maximized the reproductive output while minimizing the cost of reproduction. Received: 11 September 1997 / Accepted: 12 December 1997     

Structure and pattern in temperate seasonal forests

Demography, spatial pattern, and diversity of canopy and subcanopy trees, shrubs, and lianas were compared in two cool and two warm temperate North American forests, paired at 30° and 40° north latitudes. All woody stems 1 cm dbh in 16 randomly located, non-contiguous plots totalling 1 ha at each of the four sites were measured, mapped, and identified. Basal area and overall density did not differ between latitudes. Demographic and spatial analyses revealed remarkable similarity in spatial dispersion, irrespective of density or species composition. At all sites, dispersion of canopy trees was random but all understory stems were uniformly distributed relative to all canopy trees. Species diversity and vertical structure differed between the warm and cool temperate sites, especially in species composition of individual strata. Associations of understory species relative to canopy species were more random at 30° than at 40° north, where a higher degree of association between canopy and understory species' patterns, coupled with their size class distributions, suggested more lengthy regeneration cycles and an alternation of species assemblages. The forests at 30°, those subject to periodic canopy disturbance by hurricanes, had more vertical mixing of species (i.e., canopy species represented in all size classes), more tree saplings, and significantly more shrub and liana species.     

The responses of microbial temperature relationships to seasonal change and winter warming in a temperate grassland

Microorganisms dominate the decomposition of organic matter and their activities are strongly influenced by temperature. As the carbon (C) flux from soil to the atmosphere due to microbial activity is substantial, understanding temperature relationships of microbial processes is critical. It has been shown that microbial temperature relationships in soil correlate with the climate, and microorganisms in field experiments become more warm‐tolerant in response to chronic warming. It is also known that microbial temperature relationships reflect the seasons in aquatic ecosystems, but to date this has not been investigated in soil. Although climate change predictions suggest that temperatures will be mostly affected during winter in temperate ecosystems, no assessments exist of the responses of microbial temperature relationships to winter warming. We investigated the responses of the temperature relationships of bacterial growth, fungal growth, and respiration in a temperate grassland to seasonal change, and to 2 years’ winter warming. The warming treatments increased winter soil temperatures by 5–6°C, corresponding to 3°C warming of the mean annual temperature. Microbial temperature relationships and temperature sensitivities (Q₁₀) could be accurately established, but did not respond to winter warming or to seasonal temperature change, despite significant shifts in the microbial community structure. The lack of response to winter warming that we demonstrate, and the strong response to chronic warming treatments previously shown, together suggest that it is the peak annual soil temperature that influences the microbial temperature relationships, and that temperatures during colder seasons will have little impact. Thus, mean annual temperatures are poor predictors for microbial temperature relationships. Instead, the intensity of summer heat‐spells in temperate systems is likely to shape the microbial temperature relationships that govern the soil‐atmosphere C exchange.     

A high-copy-number CACTA family transposon in temperate grasses and cereals

A lineage of CACTA family transposons has been identified in temperate grasses and cereals, and a full-length representative of the subfamily from Lolium perenne has been sequenced. Both the size and internal organization of the L. perenne element are typical of other CACTA family elements but its high copy number and strong conservation are unexpected. Comparison with homologs in other species suggests that this lineage has adopted a distinct and novel evolutionary strategy, which has allowed it to maintain its presence in genomes over long periods of time.     

Circadian and solar clocks interact in seasonal flowering

The plant maintains a 24‐h circadian cycle that controls the sequential activation of many physiological and developmental functions. There is empirical evidence suggesting that two types of circadian rhythms exist. Some plant rhythms appear to be set by the light transition at dawn, and are calibrated to circadian (zeitgeber) time, which is measured from sunrise. Other rhythms are set by both dawn and dusk, and are calibrated to solar time that is measured from mid‐day. Rhythms on circadian timing shift seasonally in tandem with the timing of dawn that occurs earlier in summer and later in winter. On the other hand, rhythms set to solar time are maintained independently of the season, the timing of noon being constant year‐round. Various rhythms that run in‐phase and out‐of‐phase with one another seasonally may provide a means to time and induce seasonal events such as flowering.     

Control of flowering time

The multiple promotive and repressive pathways controlling flowering have been further defined by analysis of genetic interactions and the activation of floral meristem identity genes. Cloning of additional genes in these pathways has uncovered some of the molecular processes that control the timing of the transition to reproductive development.     

Salicylic acid regulates flowering time and links defence responses and reproductive development

Flowering relies on signaling networks that integrate endogenous and external cues. Normally, plants flower at a particular season, reflecting day length and/or temperature cues. However, plants can surpass this seasonal regulation and show precocious flowering under stress environmental conditions. Here, we show that UV-C light stress activates the transition to flowering in Arabidopsis thaliana through salicylic acid (SA). Moreover, SA also regulates flowering time in non-stressed plants, as SA-deficient plants are late flowering. The regulation of flowering time by SA seems to involve the photoperiod and autonomous pathways, but it does not require the function of the flowering time genes CONSTANS (CO), FCA, or FLOWERING LOCUS C (FLC).     

Integration of flowering signals in winter-annual Arabidopsis

Photoperiod is the primary environmental factor affecting flowering time in rapid-cycling accessions of Arabidopsis (Arabidopsis thaliana). Winter-annual Arabidopsis, in contrast, have both a photoperiod and a vernalization requirement for rapid flowering. In winter annuals, high levels of the floral inhibitor FLC (FLOWERING LOCUS C) suppress flowering prior to vernalization. FLC acts to delay flowering, in part, by suppressing expression of the floral promoter SOC1 (SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1). Vernalization leads to a permanent epigenetic suppression of FLC. To investigate how winter-annual accessions integrate signals from the photoperiod and vernalization pathways, we have examined activation-tagged alleles of FT and the FT homolog, TSF (TWIN SISTER OF FT), in a winter-annual background. Activation of FT or TSF strongly suppresses the FLC-mediated late-flowering phenotype of winter annuals; however, FT and TSF overexpression does not affect FLC mRNA levels. Rather, FT and TSF bypass the block to flowering created by FLC by activating SOC1 expression. We have also found that FLC acts as a dosage-dependent inhibitor of FT expression. Thus, the integration of flowering signals from the photoperiod and vernalization pathways occurs, at least in part, through the regulation of FT, TSF, and SOC1.