All in good time: Timing gene activation during early flower development

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Pelayo et al. explore the function of a biological timer that activates key genes for flowering.

Margaret Anne Pelayo, Nara Institute of Science and Technology

https://doi.org/10.1093/plcell/koad123

Background: For flowers to form, the floral meristem (floral stem cells) must irreversibly commit to becoming cells making up the various floral organs (sepals, petals, stamens, and carpels), a process known as floral meristem termination. Proper timing of floral meristem termination involves temporal activation of the transcription factor gene KNUCKLES (KNU) by its upstream regulator AGAMOUS (AG) via cell cycle-dependent dilution of the repressive histone modification at lysine 27 of histone H3 (H3K27me3) along the KNU coding sequence. This intrinsic ‘biotimer’ will activate KNU at precisely the right time to ensure proper flower development.

Question: Are there other genes similarly regulated by AGAMOUS during flower development making up a biotimer transcriptional regulatory network and can we manipulate KNU gene activation timing based on the set of criteria that defines the biotimer mechanism?

Findings: Using the model plant Arabidopsis thaliana, we found that the genes AT HOOK MOTIF NUCLEAR LOCALIZED PROTEIN18 (AHL18) and PLATZ10 are direct biotimer-regulated AG targets among a set of 23 biotimer candidate genes (including KNU). AHL18 and PLATZ10 are likely involved during stamen development, specifically for proper stamen elongation and maturation, respectively. We also introduced a simple mathematical model correlating the length of H3K27me3-marked regions at biotimer genes with gene activation timing and correctly predicted the timing of activation for KNU, AHL18, and PZ10. We validated the model’s predictions experimentally by modifying KNU gene length with tandem repeats of a H3K27me3-dense region in KNU’s coding sequence named del resulting in delayed and reduced KNU expression in a PRC2- and cell cycle–dependent manner.

Next steps: Our current work provides insight into epigenetic approaches for tunable gene expression and provides a mechanistic framework to understand which aspects of transcriptional regulatory systems can be effectively manipulated for future work aimed at enhancing plant productivity and resilience.

Reference:

Margaret Anne Pelayo, Fumi Morishita, Haruka Sawada, Kasumi Matsushita, Hideaki Iimura, Zemiao He, Liang Sheng Looi, Naoya Katagiri, Asumi Nagamori, Takamasa Suzuki, Marek Širl, Aleš Soukup, Akiko Satake, Toshiro Ito and Nobutoshi Yamaguchi (2023) AGAMOUS regulates various target genes via cell cycle–coupled H3K27me3 dilution in floral meristems and stamens. https://doi.org/10.1093/plcell/koad123

A transcriptional hub integrates multiple hormone signaling pathways in rice

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Duan et al. explore the functions of OsSHI1 in rice development.

https://doi.org/10.1093/plcell/koad130

Erchao Duan

State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural University

Background: Plant growth and development are affected by various internal and external signals during their entire life cycle. To improve their chances of surviving and reproducing, plants have evolved complex ways to coordinate their growth and stress responses via integrating hormone signaling pathways. Therefore, revealing the molecular mechanisms integrating various hormone signaling pathways is not only a fundamental biological question, but also holds great promise for molecular breeding of high-yielding and stress-resilient crops in face of climate change and increasing human population.

Questions: The multifaceted hormone-related defects of the rice short internodes1 (shi1) mutant give us a clue that the OsSHI1 gene might participate in regulating multiple hormone signaling pathways. Therefore, we asked whether and how different hormone signaling pathways are integrated by OsSHI1 at the transcriptional level during rice development.

Findings: We found that the shi1 mutant exhibits many hormone-related morphological variations, such as auxin and brassinosteroid (BR)-regulated plant development as well as abscisic acid (ABA)-mediated stress tolerance. Further functional analysis revealed that several upstream transcription factors of auxin, ABA and BR pathways bind to the promoter region of OsSHI1 to activate or inhibit its transcription. OsSHI1 protein then directly regulates several auxin and BR biosynthesis genes, thus integrating the biosynthesis of auxin and BR with ABA signal transduction to coordinate plant growth and stress adaptation. In addition, OsSHI1 also negatively regulates its own expression. These findings demonstrate that OsSHI1 is a key transcriptional hub for the integration of multiple hormone signaling pathways.

Next steps: SHI family members are essential regulators of plant development. Therefore, it is important to identify and explore their functions in other hormone pathways or stresses to fully understand the biological functions of SHI transcription factors in coordinating plant development and stress adaptation in future studies.

Reference:

Erchao Duan, Qibing Lin, Yihua Wang, Yulong Ren, Huan Xu, Yuanyan Zhang, Yunlong Wang, Xuan Teng, Hui Dong, Yupeng Wang, Xiaokang Jiang, Xiaoli Chen, Jie Lei, Hang Yang, Rongbo Chen, Ling Jiang, Haiyang Wang, and Jianmin Wan. (2023). The transcriptional hub SHORT INTERNODES1 integrates hormone signals to orchestrate rice growth and development. https://doi.org/10.1093/plcell/koad130

The enzyme that makes many algae brown

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Cao and Bai et al. reveal a conserved enzyme that makes many algae appear brown as opposed to green typical of land plants.

https://doi.org/10.1093/plcell/koad116

Graham Peers1, Martin Lohr2, Xiaobo Li3,4

1 Department of Biology, Colorado State University; Fort Collins, USA.

2 Institut für Molekulare Physiologie, Johannes Gutenberg-University; Mainz, Germany.

3 Key Laboratory of Growth Regulation and Translational Research of Zhejiang Province, School of Life Sciences, Westlake University; Hangzhou, China.

4 Institute of Biology, Westlake Institute for Advanced Study; Hangzhou, China

Background: Many algae have distinctive coloration compared to plants because of differences in their photosynthetic pigments. Brown colored algae, like diatoms and kelps, contain a carotenoid pigment called fucoxanthin that permits these algae to absorb green light that penetrates deep into the water for photosynthesis. While the structure of fucoxanthin has been known for decades, the biochemical mechanisms by which this ecologically important pigment is synthesized are only now being discovered.

Question: We set out to identify the missing enzymes responsible for the final steps in the biosynthesis of fucoxanthin.

Findings: We found that a protein predicted to be from a family of carotenoid isomerases (CRTISO5) has gained a completely novel function in the fucoxanthin-containing diatom Phaeodactylum. When this gene is disrupted using clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated nuclease 9 (Cas9)-mediated genome editing, the normally brown diatom appears green and shows a reduced light-harvesting capability and growth. We used a combination of genetics, enzyme assays and molecular structural analyses to show that CRTISO5 catalyzes the final step of fucoxanthin biosynthesis. Surprisingly, instead of serving as an isomerase, it hydrates a carbon-carbon triple bond within the precursor molecule, leading to formation of the characteristic keto group in fucoxanthin.

Next steps: Algae contain a wide variety of photosynthetic pigments that are not found in plants. Our results show that algae repeatedly repurposed pigment biosynthesis genes for novel functions and that these gene families are ripe for exploration.

Reference:

Tianjun Cao, Yu Bai, Paul Buschbeck, Qiaozhu Tan, Michael B. Cantrell, Yinjuan Chen, Yanyou Jiang, Run-Zhou Liu, Nana K. Ries, Xiaohuo Shi, Yan Sun, Maxwell A. Ware, Fenghua Yang, Huan Zhang, Jichang Han, Lihan Zhang, Jing Huang, Martin Lohr, Graham Peers, Xiaobo Li. (2023). An unexpected hydratase synthesizes the green light­-absorbing pigment fucoxanthin. https://doi.org/10.1093/plcell/koad116

Targeting of plasmodesmal proteins requires unconventional signals

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Gabriel Robles Luna, Jung-Youn Lee and colleagues discover that proteins carry targeting signals that send them to plasmodesmata, but these signals show no sequence conservation.

https://doi.org/10.1093/plcell/koad152

Gabriel Robles Luna1, Jiefu Li3, Xu Wang1, Li Liao2,3, and Jung-Youn Lee1,2,4*         

1Department of Plant and Soil Sciences, University of Delaware; Newark, DE19716, USA

2Delaware Biotechnology Institute, University of Delaware; Newark, DE19716, USA

3Department of Computer and Information Sciences, University of Delaware; Newark, DE19716, U. S. A.

4Department of Biological Sciences, University of Delaware; Newark, DE19716, USA

 Current addresses:

Instituto de Biotecnología y Biología Molecular (IBBM, CCT-CONICET-La Plata), Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Calles 115 49 y 50 (1900), Buenos Aires, La Plata, Argentina (GRL)

School of Optical-Electrical and Computer Engineering, University of Shanghai for Science and Technology, Shanghai, China; Department of Plant Physiology and Biochemistry, University of Hohenheim, 70593 Stuttgart, Germany (XW).

*Corresponding author. Email: [email protected]

Background: In plants, cells communicate through tiny membrane-lined nanotubes or nanopores called plasmodesmata, which allow molecules and signals to move between neighboring cells. These pores can change their permeability in response to various cellular stimuli or environmental challenges. Some proteins are specifically targeted to plasmodesmata to regulate this permeability, but what sends them there remains unknown.

Question: We aimed to identify the molecular determinants responsible for directing several membrane proteins, particularly PLASMODESMATA-LOCATED PROTEIN 5 (PDLP5), a key regulator of plasmodesmal permeability, to plasmodesmata. We also tested other PDLP family members and other membrane proteins unrelated to PDLP proteins for potential conservation of targeting signals. These aims were quite challenging due to the lack of known examples.

Findings: We combined machine-learning algorithms with targeted mutagenesis and deletions. We discovered that PDLP5 and its related proteins in Arabidopsis (Arabidopsis thaliana) and Nicotiana benthamiana contain unconventional targeting signals in their extracellular regions. These targeting signals consist of short stretches that vary in sequence but share a similar location near the membrane. These signals are crucial for PDLP5 localization and biological function in regulating viral movement. We also found that several receptor kinases that localize to plasmodesmata require a similarly located extracellular region near the membrane for specific targeting to plasmodesmata. Finally, we showed that the targeting signal of PDLP5 can redirect plasma membrane-localized receptor kinases to plasmodesmata.

Next steps: What are the molecular mechanisms behind the targeting of proteins to plasmodesmata? We hope to uncover the specific transport machinery and potential cognate receptors involved, advancing our understanding of plant cellular communication and providing insights for potential applications in agriculture and plant biotechnology.

Reference: 

Gabriel Robles Luna, Jiefu Li, Xu Wang, Li Liao, and Jung-Youn Lee (2023). Targeting of plasmodesmal proteins requires unconventional signals. https://doi.org/10.1093/plcell/koad152

Nascent pri-miRNAs and HYL1 act as a scaffold to recruit transcriptional regulators to miRNA loci

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Park et al. reveal how a microprocessor component and a histone deacetylase act in microRNA biogenesis under stress.

Background: MicroRNAs (miRNAs) are small noncoding RNAs with a length of 21–24 nucleotides that play critical roles in mRNA silencing and translational suppression. In plants, miRNAs are transcribed by RNA polymerase II and processed by the microprocessor, which includes HYPONASTIC LEAVES 1 (HYL1) as a core factor. To maintain homeostasis in the plants and ensure proper developmental programming, the microprocessor is tightly regulated at the transcriptional and post-transcriptional levels. This regulation is particularly important when the plants face environmental stresses, and miRNAs function as key regulatory elements.

Question: A forward genetic screen identified the HOS15-HISTONE DEACETYLASE9 (HDA9) complex, a well-defined stress-responsive complex, as a component of miRNA biogenesis that interacts with HYL1. We therefore wondered how the HOS15-HDA9 complex acts in the miRNA pathway, how HYL1 is involved in this process, and whether this regulation is important during signaling of the stress-related hormone abscisic acid (ABA).

Findings: We showed that the HOS15-HDA9 complex is a conditional suppressor of miRNA biogenesis under ABA treatment in Arabidopsis thaliana. HYL1 recognizes the nascent primary miRNAs (pri-miRNAs) and guides the HOS15-HDA9 complex to miRNA gene loci. This recruitment suppresses miRNA gene expression and pri-miRNA processing. hos15 hda9 mutants show an increase in pri-miRNA transcription and processing that leads to the over-accumulation of a set of mature miRNAs. Thus, our findings indicate that the nascent pri-miRNAs could serve as scaffolds for recruiting transcriptional regulators specifically to miRNA gene loci.

Next steps: Defining why only a subset of miRNAs appears to be affected by the HOS15-HDA9 complex, even under ABA treatment, is a compelling open question. Additionally, understanding the precise molecular mechanism by which the HOS15-HDA9 complex suppresses pri-miRNA processing requires further investigation.

Reference:

Junghoon Park, Axel J. Giudicatti, Zein Eddin Bader, Min Kyun Han, Christian Møller, Agustin L. Arce, Zheng-Yi Xu, Seong Wook Yang, Pablo A. Manavella, Dae-Jin Yun (2023) The HOS15-HDA9 complex associates with HYL1 to modulate miRNA expression in response to ABA signaling. https://doi.org/10.1093/plcell/koad132

Review: Rapid auxin signaling: Unknowns old and new

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You might think you’ve read enough about auxin, but I recommend you take this opportunity to read one more article, this very interesting and enjoyable review by Fielder and Friml. Auxin has figured prominently in both the classical and molecular eras of plant biology. However, the exciting findings of auxin’s transcriptional responses through the TIR1 auxin receptor relatively early in the molecular era really dominated the field over the past 25 years, overshadowing the classically-described “fast” auxin responses that aren’t explained by transcription. Further complications arose when it was revealed that the effects ascribed to Auxin Binding Protein 1 through analysis of the Arabidopsis abp1 mutant were not quite as they seemed. It’s not an overstatement to say, as the authors do, that this finding “poured fuel on the fire of a community that was already, as human nature sometimes dictates, divided by its favoritism for either ABP1 or TIR1 as the more relevant auxin receptor.” That’s enough foreshadowing, so please turn to the article for the rest of this elegantly constructed update. (Summary by Mary Williams @PlantTeaching) Curr. Opin. Plant Biol. 10.1016/j.pbi.2023.102443

Review: Genome evolution in plants and the origins of innovation

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Land plants have enormous diversity; however we do not fully understand how this has arisen. In this review article James Clark discusses how genome dynamics and gene loss contribute to genome evolution and the generation of diversity and complexity. He explains how genome evolution is non-homogenous across time with specific periods where plants underwent rapid evolution. One period is the emergence of land plants, where there was an expansion of pre-existing gene families and the generation of novel gene families to allow the colonization of the land. In this process horizontal gene transfer played an important role, particularly for the evolution of genes involved in stress response. In addition to gene gain, gene loss has had a major influence on plant evolution, particularly within bryophytes.  One example is the genes involved in stomata formation, which were present in a bryophyte ancestor but have since been lost in liverworts and some mosses and hornworts. This loss has led to generation of phenotypic diversity for instance the development of the novel gas exchange structure, the air pore, in liverworts. Hence, Clark argues that gene loss plays a significant role in generating diversity and needs to be carefully considered in plant evolution. (Summary by Rose McNully @Rose_McN) New Phytol.  10.1111/nph.19242

Review: Improving RNA-based crop protection through nanotechnology and insights from cross-kingdom RNA trafficking

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The German physician Paul Ehrlich (not to be confused with the American scientist of the same name) coined the term “magic bullet” (zauberkugel) to describe something that is perfectly and accurately effective. As much as we dream of magic bullets, they are rarely found, but the idea of using spray-on RNA as an agent of pest control seems pretty close. Here, Chen et al. review progress in this field, specifically spray-induced gene silencing (SIGS), and particularly the use of nanotechnology to improve its efficacy. The potential for small RNAs to specifically and effectively silence target genes has been recognized for decades; the challenges in pest control are largely about delivery and stability. The authors review examples of naturally occurring cross-kingdom RNAi, particularly the involvement of extracellular vesicles in enabling movement. Delivery and stability are greatly increased by the encapsulation of the RNA into nanoparticles of various design and composition (including layered double hydroxide clay nanosheets, chitosan, carbon-based materials, liposomes, and star polycations). There’s an interesting discussion about how the nanoparticles enter the plant, and translocation within the plant tissues, and efforts to improve these. Before widely adopted, the fate of the nanocarriers in the environment and impacts on non-target organisms needs to be addressed. Nevertheless, the appeal of spraying on droplets of encapsulated, highly targeted small RNAs as a means of crop protection is real. (Summary by Mary Williams @PlantTeaching) Curr. Opin. Plant Biol. 10.1016/j.pbi.2023.102441

Commentary: Time to fight the over-hype

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A year ago, graduate student Merritt Khaipho-Burch Tweeted a reaction to an article about a gene described as enhancing yield, which led to lively on-line and in-the-lunchroom discussions about how to realistically measure yield, and, maybe more importantly, where to draw the line between potential and promise. Now, Khaipho-Burch and colleagues have published a set of recommendations for researchers, reviewers, and editors, to cast a more realistic and critical view towards research efforts to improve crop yields. Their five recommendations: Standard definition of yield; Broad replication; Farm-like conditions; Appropriate controls; and Priority to genes breeders might have missed. On this last point, the authors state, “If plant breeders have already worked with a gene for decades, it is extremely unlikely that it will suddenly deliver major yield gains.” Needless to say, this is a much-needed commentary that should be discussed at your next lab meeting. (Summary by Mary Williams @PlantTeaching) Nature 10.1038/d41586-023-02895-w