Spatio-temporal analysis of strawberry architecture: insights into the control of branching and inflorescence complexity.

Plant architecture plays a major role in flowering and therefore in crop yield. Attempts to visualize and analyse strawberry plant architecture have been few to date. Here, we developed open-source software combining two- and three-dimensional representations of plant development over time along with statistical methods to explore the variability in spatio-temporal development of plant architecture in cultivated strawberry. We applied this software to six seasonal strawberry varieties whose plants were exhaustively described monthly at the node scale. Results showed that the architectural pattern of the strawberry plant is characterized by a decrease of the module complexity between the zeroth-order module (primary crown) and higher-order modules (lateral branch crowns and extension crowns). Furthermore, for each variety, we could identify traits with a central role in determining yield, such as date of appearance and number of branches. By modeling the spatial organization of axillary meristem fate on the zeroth-order module using a hidden hybrid Markov/semi-Markov mathematical model, we further identified three zones with different probabilities of production of branch crowns, dormant buds, or stolons. This open-source software will be of value to the scientific community and breeders in studying the influence of environmental and genetic cues on strawberry architecture and yield.

The FveFT2 florigen/FveTFL1 antiflorigen balance is critical for the control of seasonal flowering in strawberry while FveFT3 modulates axillary meristem fate and yield.

Plant architecture is central in determining crop yield. In the short-day species strawberry, a crop vegetatively propagated by daughter-plants produced by stolons, fruit yield is further dependent on the trade-off between sexual reproduction (fruits) and asexual reproduction (daughter-plants). Both are largely dependent on meristem identity, which establishes the development of branches, stolons and inflorescences. Floral initiation and plant architecture are modulated by the balance between two related proteins, FLOWERING LOCUS T (FT) and TERMINAL FLOWER 1 (TFL1). We explored in woodland strawberry the role of the uncharacterised FveFT2 and FveFT3 genes and of the floral repressor FveTFL1 through gene expression analyses, grafting and genetic transformation (overexpression and gene editing). We demonstrate the unusual properties of these genes. FveFT2 is a nonphotoperiodic florigen permitting short-day (SD) flowering and FveTFL1 is the long-hypothesised long-day systemic antiflorigen that contributes, together with FveFT2, to the photoperiodic regulation of flowering. We additionally show that FveFT3 is not a florigen but promotes plant branching when overexpressed, that is likely to be through changing axillary meristem fate, therefore resulting in a 3.5-fold increase in fruit yield at the expense of stolons. We show that our findings can be translated into improvement of cultivated strawberry in which FveFT2 overexpression significantly accelerates flowering.

A Specific Gibberellin 20-Oxidase Dictates the Flowering-Runnering Decision in Diploid Strawberry.

Asexual and sexual reproduction occur jointly in many angiosperms. Stolons (elongated stems) are used for asexual reproduction in the crop species potato (Solanum tuberosum) and strawberry (Fragaria spp), where they produce tubers and clonal plants, respectively. In strawberry, stolon production is essential for vegetative propagation at the expense of fruit yield, but the underlying molecular mechanisms are unknown. Here, we show that the stolon deficiency trait of the runnerless (r) natural mutant in woodland diploid strawberry (Fragaria vesca) is due to a deletion in the active site of a gibberellin20-oxidase (GA20ox) gene, which is expressed primarily in the axillary meristem dome and primordia and in developing stolons. This mutation, which is found in all r mutants, goes back more than three centuries. When FveGA20ox4 is mutated, axillary meristems remain dormant or produce secondary shoots terminated by inflorescences, thus increasing the number of inflorescences in the plant. The application of bioactive gibberellin (GA) restored the runnering phenotype in the r mutant, indicating that GA biosynthesis in the axillary meristem is essential for inducing stolon differentiation. The possibility of regulating the runnering-flowering decision in strawberry via FveGA20ox4 provides a path for improving productivity in strawberry by controlling the trade-off between sexual reproduction and vegetative propagation.

Identifying phenological phases in strawberry using multiple change-point models.

Plant development studies often generate data in the form of multivariate time series, each variable corresponding to a count of newly emerged organs for a given development process. These phenological data often exhibit highly structured patterns, and the aim of this study was to identify such patterns in cultivated strawberry. Six strawberry genotypes were observed weekly for their course of emergence of flowers, leaves, and stolons during 7 months. We assumed that these phenological series take the form of successive phases, synchronous between individuals. We applied univariate multiple change-point models for the identification of flowering, vegetative development, and runnering phases, and multivariate multiple change-point models for the identification of consensus phases for these three development processes. We showed that the flowering and the runnering processes are the main determinants of the phenological pattern. On this basis, we propose a typology of the six genotypes in the form of a hierarchical classification. This study introduces a new longitudinal data modeling approach for the identification of phenological phases in plant development. The focus was on development variables but the approach can be directly extended to growth variables and to multivariate series combining growth and development variables.

High Resolution Quantitative Trait Locus Mapping and Whole Genome Sequencing Enable the Design of an Anthocyanidin Reductase-Specific Homoeo-Allelic Marker for Fruit Colour Improvement in Octoploid Strawberry (Fragaria × ananassa).

Fruit colour is central to the sensorial and nutritional quality of strawberry fruit and is therefore a major target in breeding programmes of the octoploid cultivated strawberry (Fragaria × ananassa). The red colour of the fruit is caused by the accumulation of anthocyanins, which are water-soluble flavonoids. To facilitate molecular breeding, here we have mapped with high resolution fruit colour quantitative trait loci (QTLs) (COLOUR, scored visually as in selection programmes) and associated flavonoid metabolic QTLs (5 anthocyanins compounds together with 8 flavonols and flavan-3-ols) to specific subgenomes of cultivated strawberry. Two main colour-related QTLs were located on the LG3A linkage group (Fragaria vesca subgenome). Genetic mapping, transcriptome analysis and whole genome sequencing enabled the detection of a homoeo-allelic variant of ANTHOCYANIDIN REDUCTASE (ANR) underlying the major male M3A COLOUR and pelargonidin-3-glucoside (PgGs) QTLs (up to ∼20% of explained variance). Consistent with previously published functional studies, ANR transcript abundance was inversely related with PgGs content in contrasted progeny individuals. Genetic segregation analyses further indicated that a molecular marker designed using an 18 bp deletion found in the 5'UTR of the candidate ANR homoeo-allelic variant is effective in identifying genotypes with intense red fruit colour. Our study provides insights into the genetic and molecular control of colour-related traits in strawberry and further defines a genetic marker for marker-assisted selection of new strawberry varieties with improved colour. The QTLs detected and the underlying candidate genes are different from those described to date, emphasising the importance of screening a wide diversity of genetic resources in strawberry.

Metabolite Quantitative Trait Loci for Flavonoids Provide New Insights into the Genetic Architecture of Strawberry (Fragaria × ananassa) Fruit Quality.

Flavonoids are products from specialized metabolism that contribute to fruit sensorial (color) and nutritional (antioxidant properties) quality. Here, using a pseudo full-sibling F1 progeny previously studied for fruit sensorial quality of cultivated strawberry (Fragaria × ananassa), we explored over two successive years the genetic architecture of flavonoid-related traits using liquid chromatography electrospray ionization tandem mass spectrometry (13 compounds including anthocyanins, flavonols, and flavan-3-ols) and colorimetric assays (anthocyanins, flavonoids, phenolics, and total antioxidant capacity (ferric reducing antioxidant power and Trolox equivalent antioxidant capacity)). Network correlation analysis highlighted the high connectivity of flavonoid compounds within each chemical class and low correlation with colorimetric traits except for anthocyanins. Mapping onto the female and male linkage maps of 152 flavonoid metabolic quantitative trait loci (mQTLs) and of 26 colorimetric QTLs indicated colocalization on few linkage groups of major flavonoid- and taste-related QTLs previously uncovered. These results pave the way for the discovery of genetic variations underlying flavonoid mQTLs and for marker-assisted selection of strawberry varieties with improved sensorial and nutritional quality.

Interact to survive: Phyllobacterium brassicacearum improves Arabidopsis tolerance to severe water deficit and growth recovery.

Mutualistic bacteria can alter plant phenotypes and confer new abilities to plants. Some plant growth-promoting rhizobacteria (PGPR) are known to improve both plant growth and tolerance to multiple stresses, including drought, but reports on their effects on plant survival under severe water deficits are scarce. We investigated the effect of Phyllobacterium brassicacearum STM196 strain, a PGPR isolated from the rhizosphere of oilseed rape, on survival, growth and physiological responses of Arabidopsis thaliana to severe water deficits combining destructive and non-destructive high-throughput phenotyping. Soil inoculation with STM196 greatly increased the survival rate of A. thaliana under several scenarios of severe water deficit. Photosystem II efficiency, assessed at the whole-plant level by high-throughput fluorescence imaging (Fv/Fm), was related to the probability of survival and revealed that STM196 delayed plant mortality. Inoculated surviving plants tolerated more damages to the photosynthetic tissues through a delayed dehydration and a better tolerance to low water status. Importantly, STM196 allowed a better recovery of plant growth after rewatering and stressed plants reached a similar biomass at flowering than non-stressed plants. Our results highlight the importance of plant-bacteria interactions in plant responses to severe drought and provide a new avenue of investigations to improve drought tolerance in agriculture.