A cell surface player required for dehydration signaling in foxtail millet

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Zhao, Zhang, Liu et al. identify an essential kinase for foxtail millet dehydration tolerance.

https://doi.org/10.1093/plcell/koad200

By Yuxue Zhang and Meicheng Zhao

Key Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, 050021, China

Background: To protect themselves from drought-induced damage, plants must sense the osmotic stress that accompanies drought and rapidly transmit a signal, triggering defense responses to acclimate to water deficit. When plants sense dehydration stress, SNF1-RELATED PROTEIN KINASE2 (SnRK2) family members are activated, representing a key event in dehydration signaling. Although this step was elucidated ~20 years ago, the upstream components that activate SnRK2 kinases remain unknown. We previously identified the transmembrane kinase DROOPY LEAF1 (DPY1) as a key regulator of plant architecture in foxtail millet (Setaria italica). A screen for DPY1-interacing proteins identified a member of the SnRK2 family, suggesting that DPY1 might be involved in SnRK2-mediated dehydration signaling.

Question: Is DPY1 an upstream component required for SnRK2 activation in response to dehydration stress? As a plasma membrane–anchored receptor-like kinase, how does DPY1 respond to dehydration stress?

Findings: DPY1 is crucial for plant acclimation to drought stress. Loss of DPY1 function enhanced susceptibility to drought, partially due to impaired osmotic signaling. DPY1 is phosphorylated and activated in response to osmotic stress and is required for over 50% of osmotic stress–triggered global phosphorylation events, including that of SnRK2s, the central kinases in osmotic stress. DPY1 interacts with but cannot directly phosphorylate STRESS-ACTIVATED PROTEIN KINASE6 (SAPK6), a subclass I SnRK2, but it is required for full SAPK6 activation and the regulation of downstream genes. This activation is largely independent of DPY1-mediated brassinosteroid signaling. Therefore, DPY1 is a key missing component in osmotic stress signaling that mediates SnRK2 activation when plants encounter drought stress.

Next steps: Despite the discovery of DPY1-based osmotic stress signaling, numerous gaps remain to be addressed. We plan to focus on identifying the mechanism of DPY1 activation by osmotic stress and components linking DPY1 and SnRK2s.

Reference:

Meicheng Zhao, Qi Zhang, Hong Liu, Sha Tang, Chunyue Shang, Wei Zhang, Yi Sui, Yuxue Zhang, Chunyan Zheng, Hui Zhang, Cuimei Liu, Jinfang Chu, Guanqing Jia, Haigang Wang, Xigang Liu, Diaoguo An, Feng Zhu, Hui Zhi, Chuanyin Wu and Xianmin Diao. (2023). The osmotic stress–activated receptor-like kinase DPY1 mediates SnRK2 kinase activation and drought tolerance in Setariahttps://doi.org/10.1093/plcell/koad200

ac4C modification of mRNA is required for plant development

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Wang et al. reveal the wide occurrence and biological function of N4-acetylcytidine in plant mRNA.

https://doi.org/10.1093/plcell/koad189

Huijie Liu and Mingjia Chen

College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, P.R. China

Background: Eukaryotic mRNA harbors more than 10 different chemical modifications, most of which are involved in many cellular activities such as RNA processing, RNA degradation, and translation. These chemical modifications are installed by “writer” proteins on pre-mRNA. N4-acetylcytidine (ac4C), the only known type of RNA acetylation modification, has recently been reported in mammalian mRNA. This modification is introduced by a single-copy acetyltransferase NAT10 and promotes translation efficiency.

Question: Does ac4C modification widely exist in plant mRNA and what are the biological functions of this chemical modification?

Findings: Our data demonstrate the wide occurrence of ac4C modification on RNAs from several vascular plants. Employing acRIP-seq, we mapped the distribution of ac4C modifications in Arabidopsis thaliana. We also show that Arabidopsis RNAs are acetylated by N-ACETYLTRANSFERASEs FOR CYTIDINE IN RNA 1 (ACYR1) and ACYR2, which are homologs of human NAT10. A double null mutation is embryo lethal, while abolishing three of the four ACYR alleles leads to defects in vegetative development. This phenotypic alteration is caused by the accelerated degradation of TOUGH transcript, a component of miRNA biogenesis, when its ac4C levels are reduced.

Next steps: The identification and characterization of ac4C in plant RNA give rise to the field of RNA modification and open up many research questions. Are any other proteins involved in ac4C formation and/or removal? Does ac4C modification participate in other developmental processes and/or environmental stimuli? What are the molecular mechanisms of ac4C modification regulating the target transcripts?

Wenlei Wang, Huijie Liu, Feifei Wang, Xiaoye Liu, Yu Sun, Jie Zhao, Changhua Zhu, Lijun Gan, Jinping Yu, Claus-Peter Witte, Mingjia Chen. (2023). N4-acetylation of cytidine in (m)RNA plays essential roles in plants. https://doi.org/10.1093/plcell/koad189

 

Overcoming barriers to bioengineering new disease resistance

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Bentham, De la Concepcion et al. fine-tuned a plant immune receptor pair to allow for engineering new specificities while avoiding autoactivation.

https://doi.org/10.1093/plcell/koad204

Adam R Bentham, Mark J Banfield

Department of Biochemistry and Metabolism, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK

Background: Plants use specialized intracellular immune receptors called nucleotide-binding leucine-rich repeat (NLR) to detect pathogen effector proteins secreted into the host during infection. Effectors aid plant colonization, which can result in serious disease and limit crop yields in agriculture. Therefore, immune responses triggered by NLRs upon perception of effectors are essential to maintain plants healthy. However, plant pathogens use hundreds of effectors during infection and these effectors evolve rapidly, escaping from recognition by NLR immune proteins. Recently, bioengineering of NLRs to recognize a wider range of effectors was demonstrated to be an effective means of generating disease resistant plants. However, bioengineering of NLRs can result in ‘autoactivity’ where the immune system is constantly active. This is deleterious to the health of the plant.

Question: In our study, we strived to understand the limits of bioengineering for a pair of rice NLRs called Pik. Pik are interesting NLRs as they comprise a sensor NLR (important for effector recognition) and a helper NLR (important for defense signaling). Findings: We found bioengineering of the native Pik sensor NLR often resulted in autoactivity. However, by using different combinations of Pik helper NLR alleles (an alternative form of the gene) we could mitigate the autoactivity caused by bioengineering, allowing us to generate Pik sensor NLRs with different effector recognition specificities in the model plant Nicotiana benthamiana. Our study establishes a strategy to incorporate a wider variety of effector recognition modules into the Pik NLRs without autoactivity.

Next Steps: The next step in this research is to understand whether this bioengineered resistance is transferable from model plants to stable transgenic crops, such as rice (Oryza sativa), barley (Hordeum vulgare), wheat (Triticum aestivum) or maize (Zea mays), and to understand which pathogens are the best targets for new disease resistance using the Pik NLRs.

Reference:

Adam R. Bentham, Juan Carlos De la Concepcion, Javier Vega Benjumea, Jiorgos Kourelis, Sally Jones, Melanie Mendel, Jack Stubbs, Clare E. M. Stevenson, Josephine H.R. Maidment, Mark Youles, Rafał Zdrzałek, Sophien Kamoun, Mark J. Banfield (2023) Allelic compatibility in plant immune receptors facilitates engineering of new effector recognition specificities. https://doi.org/10.1093/plcell/koad204

A regulatory loop involving FLOWERING PROMOTING FACTOR1-like proteins, VERNALIZATION1, and FLOWERING LOCUS T1 represses flowering in Brachypodium distachyon

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Liu et al. identify two proteins that repress flowering by acting on the florigen activation complex.

https://doi.org/10.1093/plcell/koad190

Background: Timely flowering is critical for plant reproductive success. FLOWERING PROMOTING FACTOR1 (FPF1), a small protein without any known domains, has been shown to promote flowering in several plants, including Arabidopsis (Arabidopsis thaliana), tobacco (Nicotiana tabacum) and rice (Oryza sativa); however, the mechanism by which FPF1 functions remains unknown.

Question: How do FPF1 and FPF1-Like (FPL) proteins regulate flowering time in the model temperate grass Brachypodium distachyon?

Findings: We characterized two B. distachyon FPF1-like proteins, FPL1 and FPL7. In contrast to FPF, which promotes flowering in several plants, FPL1 and FPL7 repress flowering under long-day conditions in B. distachyon. FPL1 and FPL7 interact with the components of the florigen activation complex and complex formation as well as its activity to restrict expression of its critical target, VERNALIZATION 1 (VRN1) expression in leaves, thereby preventing subsequent over-accumulation of FLOWERING LOCUS T 1 (FT1) at the juvenile stage to avoid premature flowering. At the late vegetative stage, VRN1 directly binds the FPL1 promoter and represses FPL1 expression as it gradually accumulates, thus allowing proper FT1 expression in leaves and ensuring sufficient florigen activation complex formation in shoot apical meristems to initiate timely flowering.

Next steps: It will be interesting to investigate additional upstream regulators and the potential transport of FPL1 and FPL7 in grasses. In addition, the function of FPL1 orthologs in other plants remains to be determined.

Shu Liu, Siyi Chen, Yang Zhou, Yuxin Shen, Zhengrui Qin, Liang Wu (2023) VERNALIZATION1 Represses FLOWERING PROMOTING FACTOR1-LIKE1 in Leaves for Timely Flowering in Brachypodium distachyon. https://doi.org/10.1093/plcell/koad190

Review: Development of organs for nutrient uptake in parasitic plants and root nodule symbiosis

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This review by Cui et al. makes the interesting comparison between the developmental processes involved in root nodule formation and haustoria formation by roots of parasitic plants. As the authors observe, both are organs that are produced for the purpose of nutrient acquisition through “intimate relationships” with other organisms, and initiation of each starts with the perception of signals released by the partner (haustorium-inducing factors or Nod factors). In the article, the authors elaborate further on the comparison between these two pathways of organogenesis. For example, both types of organ are derived from lateral roots, and formation of both is suppressed by environmental nitrogen and enhanced by the action of auxin and cytokinins. Finally, the authors suggest that a better understanding of these processes could provide opportunities to engineer synthetic organs. (Summary by Mary Williams @PlantTeaching) Curr. Opin. Plant Biol. 10.1016/j.pbi.2023.102473

Review: Complementing model species with model clades

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Without doubt, Arabidopsis thaliana has thoroughly demonstrated its usefulness as a model species. In this interesting article by Mabry et al. (with an impressive author list!), the authors propose to expand the Arabidopsis toolkit to encompass its entire order – its family of families, the Brassicales. Brassicales includes approximately 4700 species in 18 families, including the familiar Brassicaceae family (cabbages and Arabidopsis) but also Tropaeolum (nasturtiums), Caricaceae (papaya) and many more. Building a model clade of this magnitude seems ambitious, but current sequencing technologies render it feasible. In addition to the challenge of gathering genomic data that spans the many species and families, there is the additional challenge of extensive polyploidization across the order, which not only increases genome size but also leads to selective gene loss, thus making it more difficult to identify direct comparisons between genes; interestingly, several tools have been developed for addressing these challenges. The article touches on some of the biological insights (flower development, small RNAs) gleaned from Arabidopsis research and how they can be informed by comparative studies on the broader, “model clade”. There’s also discussion about looking at specialized metabolites, “woodiness”, photosynthesis, and extremophytism in the Brasicales. The article concludes with the need for an integrated, global community to work together to expand from model species to model clade. (Summary by Mary Williams @PlantTeaching) Plant Cell 10.1093/plcell/koad260

Review: Challenges to improving plant growth through introduced microbes

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Plants are closely associated with large numbers of microbes that live in, on, and around them; these are collectively called the plant microbiota. Microbes can be pathogenic, neutral, or beneficial. Beneficial microbes might enhance nutrient uptake by the plant or suppress pathogenic microbes. There is growing interest in using introduced microbes to support plant growth, but this effort is complicated by many factors. The plant defense system is of course a big challenge, but going beyond that, interactions between microbial communities provide further difficulties. The new species needs to compete with pre-existing species, and conflicts may arise that harm not only the new ones but also other beneficial microbes. Plants apply selective pressure to the microbial communities, fostering the development of microbiomes through specific immune responses to exclude pathogenesis.  The plant immune system regulates microbial balance in various manners, including hormonal signaling, immune receptor signaling and secondary metabolite production. Environmental fluctuations also pose challenges to the deployment of microbial strategies, especially factors like drought, iron deficiencies, and phosphate levels. The crosstalk between the plant immune system and other pathways, such as symbiosis and abiotic stress, further complicates this process. Although questions about how to enhance plant productivity through beneficial microbes remain, our understanding is rapidly expanding, with technologies like high-throughput assays being utilized to identify microbial traits. Innovative strategies, like using engineered microbes to carry several beneficial traits, remain to be tested in real-world scenarios. (Summary by Diwen Wang @Diwen_w) Cell 10.1016/j.cell.2023.08.035

Letter: Finding umbrella trees: Cultivating inclusion and more than survival in a post-affirmative action academy

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In this Letter to the Editor, Dr. Beronda Montgomery discusses umbrella trees (Musanga cecropioides) as metaphors for how to sustain progress after disruption, specifically the decision by the US Supreme Court to ban the use of race-conscious affirmative action in college admissions. Umbrella trees spring up in disrupted spaces and provide support when resources are scarce. As she writes, “To continue progress and mitigate attrition, new ‘umbrella trees’ that address racial representation at the systems level will need to be established and cultivated. These will require us to acknowledge and enable the active attention and interventions needed to promote equity in science, higher education, and society, more broadly.”  Clearly it is time to identify more umbrella trees as we navigate difficult times. (Summary by Mary Williams @PlantTeaching) Plant Cell 10.1093/plcell/koad261

Identifying candidates from genome wide association studies using gene orthologs

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Genome wide association studies (GWAS) identify genomic loci associated with a specific trait. However, these loci often contain many genes, so selecting which to investigate further can be tricky. To improve this Whitt, et al. developed a program called FiReMAGE (filtering results of multi-species, analogous GWAS experiments), which takes loci from many GWAS experiments conducted in different species, identifies genes under each locus, and finds orthologs. Candidate genes are those where the ortholog group is detected in multiple species. Candidate prioritization follows running the pipeline with 1000 random loci and calculating the probability that the locus overlaps with the ortholog by chance. To demonstrate the potential of this program, the authors inputted metal accumulation GWAS data from Arabidopsis thaliana, soybean (Glycine max), rice (Oryza sativa), Sorghum bicolor and maize (Zea mays). By imposing the restriction that the ortholog group had to be identified in all five species, they found 81 strong candidates. Some of these have known roles in metal accumulation, such as the molybdate transport MOT2, whilst others are novel candidates, such as a mevalonate kinase associated with iron homeostasis. Hence, this program provides a powerful way of identifying gene candidates from GWAS loci. (Summary by Rose McNelly @Rose_McN) bioRxiv https://doi.org/10.1101/2023.10.05.561051