Deciphering the evolutionary development of the "Chinese lantern" within Solanaceae.

MAIN CONCLUSION: The key genetic variation underlying the evo-devo of ICS in Solanaceae may be further pinpointed using an integrated strategy of forward and reverse genetics studies under the framework of phylogeny. The calyx of Physalis remains persistent throughout fruit development. Post-flowering, the fruiting calyx is inflated rapidly to encapsulate the berry, giving rise to a "Chinese lantern" structure called inflated calyx syndrome (ICS). It is unclear how this novelty arises. Over the past 2 decades, the role of MADS-box genes in the evolutionary development (evo-devo) of ICS has mainly been investigated within Solanaceae. In this review, we analyze the main achievements, challenges, and new progress. ICS acts as a source for fruit development, provides a microenvironment to protect fruit development, and assists in long-distance fruit dispersal. ICS is a typical post-floral trait, and the onset of its development is triggered by specific developmental signals that coincide with fertilization. These signals can be replaced by exogenous gibberellin and cytokinin application. MPF2-like heterotopic expression and MBP21-like loss have been proposed to be two essential evolutionary events for ICS origin, and manipulating the related MADS-box genes has been shown to affect the ICS size, sepal organ identity, and/or male fertility, but not completely disrupt ICS. Therefore, the core genes or key links in the ICS biosynthesis pathways may have undergone secondary mutations during evolution, or they have not yet been pinpointed. Recently, we have made some encouraging progress in acquiring lantern mutants in Physalis floridana. In addition to technological innovation, we propose an integrated strategy to further analyze the evo-devo mechanisms of ICS in Solanaceae using forward and reverse genetics studies under the framework of phylogeny.

Rice BARENTSZ genes are required to maintain floral developmental stability against temperature fluctuations.

BARENTSZ (BTZ), a core component of the exon junction complex, regulates diverse developmental processes in animals. However, its evolutionary and developmental roles in plants remain elusive. Here, we revealed that three groups of paralogous BTZ genes existed in Poaceae, and Group 2 underwent loss-of-function mutations during evolution. They showed surprisingly low (~33%) sequence identities, implying functional divergence. Two genes retained in rice, OsBTZ1 and OsBTZ3, were edited; however, the resultant osbtz1 and osbtz3 mutants showed similar floral morphological and functional defects at a low frequency. When growing under low-temperature conditions, developmental abnormalities became pronounced, and new floral variations were induced. In particular, stamen and carpel functionality was impaired in these rice btz mutants. The double-gene mutant osbtz1/3 shared these floral defects with an increased frequency, which was further induced under low-temperature conditions. OsBTZs interacted with OsMADS7 and OsMADS8, and the floral expressions of the OsTGA10 and MADS-box genes were correlatively altered in these osbtz mutants and responded to low-temperature treatment. These novel findings demonstrate that two highly diverged OsBTZs are required to maintain floral developmental stability under low-temperature conditions, and play an integral role in male and female fertility, thus providing new insights into the indispensable roles of BTZ genes in plant development and adaptive evolution.

A High-Precision Identification Method for Maize Leaf Diseases and Pests Based on LFMNet under Complex Backgrounds.

Maize, as one of the most important crops in the world, faces severe challenges from various diseases and pests. The timely and accurate identification of maize leaf diseases and pests is of great significance for ensuring agricultural production. Currently, the identification of maize leaf diseases and pests faces two key challenges: (1) In the actual process of identifying leaf diseases and pests, complex backgrounds can interfere with the identification effect. (2) The subtle features of diseases and pests are difficult to accurately extract. To address these challenges, this study proposes a maize leaf disease and pest identification model called LFMNet. Firstly, the localized multi-scale inverted residual convolutional block (LMSB) is proposed to perform preliminary down-sampling on the image, preserving important feature information for the subsequent extraction of fine disease and pest features in the model structure. Then, the feature localization bottleneck (FLB) is proposed to improve the model's ability to focus on and locate disease and pest characteristics and to reduce interference from complex backgrounds. Subsequently, the multi-hop local-feature fusion architecture (MLFFA) is proposed, which effectively addresses the problem of extracting subtle features by enhancing the extraction and fusion of global and local disease and pest features in images. After training and testing on a dataset containing 19,451 images of maize leaf diseases and pests, the LFMNet model demonstrated excellent performance, with an average identification accuracy of 95.68%, a precision of 95.91%, a recall of 95.78%, and an F1 score of 95.83%. Compared to existing models, it exhibits significant advantages, offering robust technical support for the precise identification of maize diseases and pests.

CRLNet: A Multimodal Peach Detection Network Based on Cooperative Asymptotic Enhancement and the Fusion of Granularity Refinement.

Accurate peach detection is essential for automated agronomic management, such as mechanical peach harvesting. However, ubiquitous occlusion makes identifying peaches from complex backgrounds extremely challenging. In addition, it is difficult to capture fine-grained peach features from a single RGB image, which can suffer from light and noise in scenarios with dense small target clusters and extreme light. To solve these problems, this study proposes a multimodal detector, called CRLNet, based on RGB and depth images. First, YOLOv9 was extended to design a backbone network that can extract RGB and depth features in parallel from an image. Second, to address the problem of information fusion bias, the Rough-Fine Hybrid Attention Fusion Module (RFAM) was designed to combine the advantageous information of different modes while suppressing the hollow noise at the edge of the peach. Finally, a Transformer-based Local-Global Joint Enhancement Module (LGEM) was developed to jointly enhance the local and global features of peaches using information from different modalities in order to enhance the percentage of information about the target peaches and remove the interference of redundant background information. CRLNet was trained on the Peach dataset and evaluated against other state-of-the-art methods; the model achieved an mAP50 of 97.1%. In addition, CRLNet also achieved an mAP50 of 92.4% in generalized experiments, validating its strong generalization capability. These results provide valuable insights for peach and other outdoor fruit multimodal detection.

Identification of microRNAs and their target genes associated with chasmogamous and cleistogamous flower development in Viola prionantha.

MAIN CONCLUSION: Differentially expressed microRNAs were found associated with the development of chasmogamous and cleistogamous flowers in Viola prionantha, revealing potential roles of microRNAs in the developmental evolution of dimorphic flowers. In Viola prionantha, chasmogamous (CH) flowers are induced by short daylight, while cleistogamous (CL) flowers are triggered by long daylight. How environmental factors and microRNAs (miRNAs) affect dimorphic flower formation remains unknown. In this study, small RNA sequencing was performed on CH and CL floral buds at different developmental stages in V. prionantha, differentially expressed miRNAs (DEmiRNAs) were identified, and their target genes were predicted. In CL flowers, Viola prionantha miR393 (vpr-miR393a/b) and vpr-miRN3366 were highly expressed, while in CH flowers, vpr-miRN2005, vpr-miR172e-2, vpr-miR166m-3, vpr-miR396f-2, and vpr-miR482d-2 were highly expressed. In the auxin-activated signaling pathway, vpr-miR393a/b and vpr-miRN2005 could target Vpr-TIR1/AFB and Vpr-ARF2, respectively, and other DEmiRNAs could target genes involved in the regulation of transcription, e.g., Vpr-AP2-7. Moreover, Vpr-UFO and Vpr-YAB5, the main regulators in petal and stamen development, were co-expressed with Vpr-TIR1/AFB and Vpr-ARF2 and showed lower expression in CL flowers than in CH flowers. Some V. prionantha genes relating to the stress/defense responses were co-expressed with Vpr-TIR1/AFB, Vpr-ARF2, and Vpr-AP2-7 and highly expressed in CL flowers. Therefore, in V. prionantha, CH-CL flower development may be regulated by the identified DEmiRNAs and their target genes, thus providing the first insight into the formation of dimorphic flowers in Viola.

ApoE Mimic Peptide COG1410 Reduces Aß Deposition and Improves Cognitive Function by Inducing the Transformation of A1/A2 Reactive Astrocytes and Increasing the BDNF Concentration in Brain of APP/PS1 Double Transgenic Mice.

The main clinical manifestation of Alzheimer's disease is progressive cognitive decline, and its pathological features are ß-amyloid (Aß) deposition, neurofibrillary tangles, synaptic dysfunction and neuron death. Neuroinflammation is an important reason for the occurrence and development of AD, which is mainly manifested by the accumulation of activated microglia and reactive astrocytes. Apolipoprotein E (ApoE) is one of the most important apolipoprotein in the brain, which is related to metabolism, aggregation and toxicity of Aß. However, the underlying mechanism needs to be further explored. In this study, we studied the effect of ApoE mimetic peptide COG1410 on spatial learning and memory functions, deposition of Aß in the dentate gyrus (DG) of APP/PS1 transgenic mice, and the different effects of A1 and A2 subtypes of reactive astrocytes. Administration of COG1410 effectively improved performance in spatial learning and memory of APP/PS1 mice, reduced Aß deposition and significantly reverted the ratio of A1/A2 reactive astrocytes, which could be associated with BDNF/TrkB signaling pathway. On the whole, the present findings suggest new possibility of using apolipoprotein E mimetic peptide to treat AD with potential effectiveness.

A loss-of-function mutant allele of a glycosyl hydrolase gene has been co-opted for seed weight control during soybean domestication.

The resultant DNA from loss-of-function mutation can be recruited in biological evolution and development. Here, we present such a rare and potential case of "to gain by loss" as a neomorphic mutation during soybean domestication for increasing seed weight. Using a population derived from a chromosome segment substitution line of Glycine max (SN14) and Glycine soja (ZYD06), a quantitative trait locus (QTL) of 100-seed weight (qHSW) was mapped on chromosome 11, corresponding to a truncated ß-1, 3-glucosidase (ßGlu) gene. The novel gene hsw results from a 14-bp deletion, causing a frameshift mutation and a premature stop codon in the ßGlu. In contrast to HSW, the hsw completely lost ßGlu activity and function but acquired a novel function to promote cell expansion, thus increasing seed weight. Overexpressing hsw instead of HSW produced large soybean seeds, and surprisingly, truncating hsw via gene editing further increased the seed size. We further found that the core 21-aa peptide of hsw and its variants acted as a promoter of seed size. Transcriptomic variation in these transgenic soybean lines substantiated the integration hsw into cell and seed size control. Moreover, the hsw allele underwent selection and expansion during soybean domestication and improvement. Our work cloned a likely domesticated QTL controlling soybean seed weight, revealed a novel genetic variation and mechanism in soybean domestication, and provided new insight into crop domestication and breeding, and plant evolution.

Parallel selection of loss-of-function alleles of Pdh1 orthologous genes in warm-season legumes for pod indehiscence and plasticity is related to precipitation.

Pod dehiscence facilitates seed dispersal in wild legumes but results in yield loss in cultivated legumes. The evolutionary genetics of the legume pod dehiscence trait remain largely elusive. We characterized the pod dehiscence of chromosome segment substitution lines of Glycine max crossed with Glycine soja and found that the gene underlying the predominant quantitative trait locus (QTL) of soybean pod-shattering trait was Pod dehiscence 1 (Pdh1). A few rare loss-of-function (LoF) Pdh1 alleles were identified in G. soja, while only an allele featuring a premature stop codon was selected for pod indehiscence in cultivated soybean and spread to low-precipitation regions with increased frequency. Moreover, correlated interactions among Pdh1's haplotype, gene expression, and environmental changes for the developmental plasticity of the pod dehiscence trait were revealed in G. max. We found that orthologous Pdh1 genes specifically originated in warm-season legumes and their LoF alleles were then parallel-selected during the domestication of legume crops. Our results provide insights into the convergent evolution of pod dehiscence in warm-season legumes, facilitate an understanding of the intricate interactions between genetic robustness and environmental adaptation for developmental plasticity, and guide the breeding of new legume varieties with pod indehiscence.

The origin and evolution of carpels and fruits from an evo-devo perspective.

The flower is an evolutionary innovation in angiosperms that drives the evolution of biodiversity. The carpel is integral to a flower and develops into fruits after fertilization, while the perianth, consisting of the calyx and corolla, is decorative to facilitate pollination and protect the internal organs, including the carpels and stamens. Therefore, the nature of flower origin is carpel and stamen origin, which represents one of the greatest and fundamental unresolved issues in plant evolutionary biology. Here, we briefly summarize the main progress and key genes identified for understanding floral development, focusing on the origin and development of the carpels. Floral ABC models have played pioneering roles in elucidating flower development, but remain insufficient for resolving flower and carpel origin. The genetic basis for carpel origin and subsequent diversification leading to fruit diversity also remains elusive. Based on current research progress and technological advances, simplified floral models and integrative evolutionary-developmental (evo-devo) strategies are proposed for elucidating the genetics of carpel origin and fruit evolution. Stepwise birth of a few master regulatory genes and subsequent functional diversification might play a pivotal role in these evolutionary processes. Among the identified transcription factors, AGAMOUS (AG) and CRABS CLAW (CRC) may be the two core regulatory genes for carpel origin as they determine carpel organ identity, determinacy, and functionality. Therefore, a comparative identification of their protein-protein interactions and downstream target genes between flowering and non-flowering plants from an evo-devo perspective may be primary projects for elucidating carpel origin and development.

An enhancing effect attributed to a nonsynonymous mutation in SOYBEAN SEED SIZE 1, a SPINDLY-like gene, is exploited in soybean domestication and improvement.

Soybean (Glycine max) was domesticated from its wild relative Glycine soja. One-hundred-seed weight is one of the most important domesticated traits determining soybean yield; however, its underlying genetic basis remains elusive. We characterized a soybean seed size 1 (sss1) mutant featuring large seeds compared to its wild-type background. Positional cloning revealed that the candidate gene GmSSS1 encoded a SPINDLY homolog and was co-located in a well-identified quantitative trait locus (QTL)-rich region on chromosome 19. Knocking out GmSSS1 resulted in small seeds, while overexpressing GmSSS1/Gmsss1 induced large seeds. Modulating GmSSS1/Gmsss1 in transgenic plants can positively influence cell expansion and cell division. Relative to GmSSS1, one mutation leading to an E to Q substitution at the 182nd residue in Gmsss1 conferred an enhancing effect on seed weight. GmSSS1 underwent diversification in wild-type and cultivated soybean, and the alleles encoding the Gmsss1-type substitution of 182nd -Q, which originated along the central and downstream parts of the Yellow River, were selected and expanded during soybean domestication and improvement. We cloned the causative gene for the sss1 mutant, which is linked with a seed weight QTL, identified an elite allele of this gene for increasing seed weight, and provided new insights into soybean domestication and breeding.

Transcriptomic comparison sheds new light on regulatory networks for dimorphic flower development in response to photoperiod in Viola prionantha.

BACKGROUND: Chasmogamous (CH)-cleistogamous (CL) dimorphic flowers are developed in Viola prionantha. However, the environmental and genetic factors necessary for the CH-CL transition are unknown. RESULTS: In the present work, short-day (SD) conditions induced CH flowers, whereas long days (LDs) triggered CL flowers in V. prionantha. Compared to fully developed CH flowers, CL flowers had less mature stamens, no nectar glands, and immature petals. Comparative transcriptomics revealed differentially expressed genes (DEGs) during CL and CH development. Core genes in the photoperiod pathway, such as V. prionantha orthologs of GIGANTEA (GI), CONSTANS (CO), and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), which promote floral induction, were highly expressed in CL flowers, whereas UNUSUAL FLORAL ORGANS (UFO) and B-class MADS-box genes for floral organ identity and development showed an opposite alteration. Moreover, genes in the glycolytic process, sucrose metabolic process, and fatty acid biosynthetic process were all highly expressed in CH flowers. Interestingly, V. prionantha orthologs of the B-class MADS-box genes APETALA3 (AP3) and PISTILLATA (PI) might relate to these sugar-fatty acid processes and were co-expressed with GAIP-B-like and YABBY5 (YAB5), which regulate the development of the petal, stamen, and nectary. Compared to CH flowers, DEGs and hub genes in the most significantly correlated modules of the gene co-expression network, which are involved in abiotic and biotic responses, were upregulated in CL flowers. CONCLUSIONS: We proposed an integrative model for transcription regulation of genes in the photoperiod pathway, floral organ development, stress response, and sugar-fatty acid processes to determine CH-CL flower development in V. prionantha. Particularly, under LDs, activated GI may induce genes involved in the stress-response pathways, and then downregulated AP3 and PI or UFO to inhibit the sugar-fatty acid metabolic processes, together forming CL flowers. In contrast, CH flowers were produced under SDs. This work provides novel insights into the developmental evolution of dimorphic flowers in Viola.

A lineage-specific arginine in POS1 is required for fruit size control in Physaleae (Solanaceae) via gene co-option.

Solanaceae have important economic value mainly due to their edible fruits. Physalis organ size 1/cytokinin response factor 3 (POS1/CRF3), a unique gene in Solanaceae, is involved in fruit size variation in Physalis but not in Solanum. However, the underlying mechanisms remain elusive. Here, we found that POS1/CRF3 was likely created via the fusion of CRF7 and CRF8 duplicates. Multiple genetic manipulations revealed that only POS1 and Capsicum POS1 (CaPOS1) functioned in fruit size control via the positive regulation of cell expansion. Comparative studies in a phylogenetic framework showed the directional enhancement of POS1-like expression in the flowers and fruits of Physaleae and the specific gain of certain interacting proteins associated with cell expansion by POS1 and CaPOS1. A lineage-specific single nucleotide polymorphism (SNP) caused the 68th amino acid histidine in the POS1 orthologs of non-Physaleae (Nicotiana and Solanum) to change to arginine in Physaleae (Physalis and Capsicum). Substituting the arginine in Physaleae POS1-like by histidine completely abolished their function in the fruits and the protein-protein interaction (PPI) with calreticulin-3. Transcriptomic comparison revealed the potential downstream pathways of POS1, including the brassinosteroid biosynthesis pathway. However, POS1-like may have functioned ancestrally in abiotic stress within Solanaceae. Our work demonstrated that heterometric expression and a SNP caused a single amino acid change to establish new PPIs, which contributed to the co-option of POS1 in multiple regulatory pathways to regulate cell expansion and thus fruit size in Physaleae. These results provide new insights into fruit morphological evolution and fruit yield control.

The Physalis floridana genome provides insights into the biochemical and morphological evolution of Physalis fruits.

The fruits of Physalis (Solanaceae) have a unique structure, a lantern-like fruiting calyx known as inflated calyx syndrome (ICS) or the Chinese lantern, and are rich in steroid-related compounds. However, the genetic variations underlying the origin of these characteristic traits and diversity in Physalis remain largely unknown. Here, we present a high-quality chromosome-level reference genome assembly of Physalis floridana (~1.40 Gb in size) with a contig N50 of ~4.87 Mb. Through evolutionary genomics and experimental approaches, we found that the loss of the SEP-like MADS-box gene MBP21 subclade is likely a key mutation that, together with the previously revealed mutation affecting floral MPF2 expression, might have contributed to the origination of ICS in Physaleae, suggesting that the origination of a morphological novelty may have resulted from an evolutionary scenario in which one mutation compensated for another deleterious mutation. Moreover, the significant expansion of squalene epoxidase genes is potentially associated with the natural variation of steroid-related compounds in Physalis fruits. The results reveal the importance of gene gains (duplication) and/or subsequent losses as genetic bases of the evolution of distinct fruit traits, and the data serve as a valuable resource for the evolutionary genetics and breeding of solanaceous crops.

Multiple and integrated functions of floral C-class MADS-box genes in flower and fruit development of Physalis floridana.

KEY MESSAGE: This work reveals potentially multiple and integrated roles in flower and fruit development of floral C-class MADS-box genes in Physalis. The Physalis fruit features a morphological novelty, the Chinese lantern. Floral C-class MADS-domain AGAMOUS-like (AG-like) proteins can interact with the identified regulators of this novel structure. However, the developmental role of the floral C-class genes is unknown in Physalis. Here, we characterized two AG-like genes from Physalis floridana, designated PFAG1 and PFAG2. The two paralogous genes shared around 61.0% of sequence identity and had similar expression domains, with different expression levels in the floral and berry development. However, the genes had distinct expression patterns in leaf and calyx development. Protein-protein interaction analyses revealed that PFAG1 and PFAG2 could commonly or specifically dimerize with certain floral MADS-domain proteins as well as non-MADS-domain proteins involved in various floral developmental processes. Gene downregulation analyses demonstrated that PFAG1 may repress PFAG2, but PFAG2 did not affect PFAG1. Downregulating PFAG1 led to incomplete floral homeotic variation in the stamens and carpels, and alteration of petal coloration pattern, while downregulating PFAG2 did not result in any floral homeotic variation. PFAG1 affected pollen maturation, while PFAG2 affected female fertility. However, simultaneously downregulating PFAG1 and PFAG2 caused loss of the complete C-function, indicating that the two PFAG genes interact to determine the identity and functionality of androecia and gynoecia organs. Their potential roles in regulating fruit size and the Chinese lantern are also discussed. Our results reveal functional divergence of floral C-class MADS-box genes in Physalis, demonstrating that they may play multiple and integrated roles in flower and fruit development.

Physalis floridana CRABS CLAW mediates neofunctionalization of GLOBOSA genes in carpel development.

Floral B-function MADS-box genes, such as GLOBOSA (GLO), function in corolla and stamen organ identity specification. The functions of these genes outside these floral whorls are rarely reported. DOLL1 is a GLO gene controlling corolla and androecium organ identity. In this study we found that, in Physalis floridana double-layered-lantern 1 (doll1) mutant pollinated with wild-type pollen, fruit set was extremely low, indicating that doll1 females are dysfunctional. Stigma and style structure, stigma receptivity, pollen tube guidance, and embryo sac development were also impaired in doll1. P. floridana CRABS CLAW (PFCRC), predominantly expressed in carpels, was repressed in doll1 native carpels. Loss-of-function of PFCRC altered carpel meristem determinacy, carpel closure, and ovule number, and the resultant 'pistil' consisted of multiple spirally-arranged dorsiventral carpels occasionally with 1-2 naked ovules on the margin and trichomes at each mutated carpel tip, implying an alteration of carpel organ identity. Regulatory and genetic interactions between B-class MADS-box genes and PFCRC were revealed in a context-dependent manner in floral development. Our work reveals a new role for the B-function genes in carpel and ovule development via regulating PFCRC, providing a new understanding of genetic regulatory networks between MADS-domain and CRC transcription factors in mediating carpel organ specification, functionality, and origin.

Gibberellins are required for dimorphic flower development in Viola philippica.

Photoperiod is a major determinant of chasmogamous (CH)-cleistogamous (CL) dimorphic flower development in Viola philippica, and only long-day (LD) conditions induce CL flowers. In this study, it was found that the active gibberellin (GA) content in CL floral buds was higher than in CH floral buds formed under short-day (SD) conditions, suggesting that the biosynthesis of active GAs is enhanced by a longer photoperiod and may be associated with dimorphic flower development. Thus, the next step was to molecularly characterize the key V. philippica GA synthesis genes GA 20-oxidase (VpGA20ox) and GA 3-oxidase (VpGA3ox). In terms of the expression of VpGA20ox and VpGA3ox, it was found that the active GAs could be upregulated in developing pistils under both LD and SD conditions to develop functional pistils, and GAs could also accumulate in the stamens under SD conditions. The anthers and the adjacent petals were well developed under SD conditions. In contrast, the above-mentioned floral organs displayed low GA contents under LD conditions and were poorly developed. Although the application of paclobutrazol, an inhibitor of GA synthesis, did not reverse CL development under LD conditions, exogenous GAs could partially trigger the transition from CH to CL flowers under relative SD conditions (≤12 h daylight). This was coupled with the downregulation of B-class MADS-box genes, thereby restraining stamen and petal development. Both VpGA20ox and VpGA3ox exhibited similar expression profiles with B-class MADS-box genes in the development of the stamens and petals. Therefore, in response to photoperiod, GA signaling could affect the expression of B-class homeotic genes and regulate dimorphic flower development in Viola. As a compensation for poorly-developed nectaries, anthers, and petals, filament elongation, style shortness, and inward bending could ensure self-pollination in CL flowers. This work provides new insights into the regulation of CH-CL floral development and the evolutionary significance of the formation of dimorphic flowers.

Transcriptomic variation of the flower-fruit transition in Physalis and Solanum.

MAIN CONCLUSION: Gene expression variations in response to fertilization between Physalis and Solanum might play essential roles in species divergence and fruit evolution. Fertilization triggers variation in fruit development and morphology. The Chinese lantern, a morphological novelty derived from the calyx, is formed upon fertilization in Physalis but is not observed in Solanum. The underlying genetic variations are largely unknown. Here, we documented the developmental and morphological differences in the flower and fruit between Physalis floridana and Solanum pimpinellifolium and then evaluated both the transcript sequence variation and gene expression at the transcriptomic level at fertilization between the two species. In Physalis transcriptomic analysis, 468 unigenes were identified as differentially expressed genes (DEGs) that were strongly regulated by fertilization across 3 years. In comparison with tomato, 14,536 strict single-copy orthologous gene pairs were identified between P. floridana and S. pimpinellifolium in the flower-fruit transcriptome. Nine types of gene variations with specific GO-enriched patterns were identified, covering 58.82% orthologous gene pairs that were DEGs in either trend or dosage at the flower-fruit transition between the two species, which could adequately distinguish Solanum and Physalis, implying that differential gene expression at fertilization might play essential roles during the divergence and fruit evolution of Solanum-Physalis. Virus-induced gene silencing analyses revealed the developmental roles of some transcription factor genes in fertility, Chinese lantern development, and fruit weight control in Physalis. This study presents the first floral transcriptomic resource of Physalis, and reveals some candidate genetic variations accounting for the early fruit developmental evolution in Physalis in comparison to Solanum.

The PHOSPHATE1 genes participate in salt and Pi signaling pathways and play adaptive roles during soybean evolution.

BACKGROUND: The PHOSPHATE1 (PHO1) gene family plays diverse roles in inorganic phosphate (Pi) transfer and signal transduction, and plant development. However, the functions and diversification of soybean PHO1 family are poorly understood. RESULTS: Cultivated soybean (Glycine max) was domesticated from wild soybean (Glycine soja). To illuminate their roles in this evolutionary process, we comparatively investigated the G. max PHO1 genes (GmPHO1) in Suinong 14 (SN14) and G. soja PHO1 genes (GsPHO1) in ZYD00006 (ZYD6). The sequences of the orthologous Gm-GsPHO1 pairs were grouped into two Classes. The expression of Class I in both SN14 and ZYD6 was widely but relatively high in developing fruits, whereas Class II was predominantly expressed in the roots. The whole family displayed diverse response patterns to salt stresses and Pi-starvation in roots. Between SN14 and ZYD6, most PHO1 genes responded similarly to salinity stresses, and half had sharp contrasts in response to Pi-starvation, which corroborated the differential response capacities to salinity and low-Pi stress between SN14 and ZYD6. Furthermore, in transgenic Arabidopsis plants, most Class II members and GmPHO1;H9 from Class I could enhance salt tolerance, while only two Class II genes (GmPHO1;H4 and GmPHO1;H8) differently altered sensitivity to Pi-starvation. The expression of critical genes was accordingly altered in either salt or Pi signaling pathways in transgenic Arabidopsis plants. CONCLUSIONS: Our work identifies some PHO1 genes as promising genetic materials for soybean improvement, and suggests that expression variation is decisive to functional divergence of the orthologous Gm-GsPHO1 pairs, which plays an adaptive role during soybean evolution.

Chinese lantern in Physalis is an advantageous morphological novelty and improves plant fitness.

The origin of morphological novelties is an important but neglected issue of evolutionary biology. The fruit of the genus Physalis, a berry, is encapsulated by a novel morphological feature of the post-floral, accrescent calyx that is referred to as a Chinese lantern. The evolutionary developmental genetics of the Chinese lantern have been investigated in the last decade; however, the selective values of the morphological novelty remain elusive. Here, we measured the photosynthetic parameters of the fruiting calyces, monitored microclimatic variation within the Chinese lanterns during fruit development, performed floral-calyx-removal experiments, and recorded the fitness-related traits in Physalis floridana. Ultimately, we show that the green-fruiting calyx of Physalis has photosynthetic capabilities, thus serving as an energy source for fruit development. Moreover, the developing Chinese lantern provides a microclimate that benefits the development and maturation of berry and seed, and it improves plant fitness in terms of fruit/seed weight and number, and fruit maturation under low-temperature environments. Furthermore, the lantern structure facilitates the dispersal of fruits and seeds by water and wind. Our results suggest that the Chinese lantern morphology of Physalis is an evolutionary adaptive trait and improves plant fitness, thus providing new insight into the origin of morphological novelties.

Exon junction complex (EJC) core genes play multiple developmental roles in Physalis floridana.

KEY MESSAGE: Molecular and functional characterization of four gene families of the Physalis exon junction complex (EJC) core improved our understanding of the evolution and function of EJC core genes in plants. The exon junction complex (EJC) plays significant roles in posttranscriptional regulation of genes in eukaryotes. However, its developmental roles in plants are poorly known. We characterized four EJC core genes from Physalis floridana that were named PFMAGO, PFY14, PFeIF4AIII and PFBTZ. They shared a similar phylogenetic topology and were expressed in all examined organs. PFMAGO, PFY14 and PFeIF4AIII were localized in both the nucleus and cytoplasm while PFBTZ was mainly localized in the cytoplasm. No protein homodimerization was observed, but they could form heterodimers excluding the PFY14-PFBTZ heterodimerization. Virus-induced gene silencing (VIGS) of PFMAGO or PFY14 aborted pollen development and resulted in low plant survival due to a leaf-blight-like phenotype in the shoot apex. Carpel functionality was also impaired in the PFY14 knockdowns, whereas pollen maturation was uniquely affected in PFBTZ-VIGS plants. Once PFeIF4AIII was strongly downregulated, plant survival was reduced via a decomposing root collar after flowering and Chinese lantern morphology was distorted. The expression of Physalis orthologous genes in the DYT1-TDF1-AMS-bHLH91 regulatory cascade that is associated with pollen maturation was significantly downregulated in PFMAGO-, PFY14- and PFBTZ-VIGS flowers. Intron-retention in the transcripts of P. floridana dysfunctional tapetum1 (PFDYT1) occurred in these mutated flowers. Additionally, the expression level of WRKY genes in defense-related pathways in the shoot apex of PFMAGO- or PFY14-VIGS plants and in the root collar of PFeIF4AIII-VIGS plants was significantly downregulated. Taken together, the Physalis EJC core genes play multiple roles including a conserved role in male fertility and newly discovered roles in Chinese lantern development, carpel functionality and defense-related processes. These data increase our understanding of the evolution and functions of EJC core genes in plants.