In tune with power: Mitochondrial regulation of energy with TOR

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As seedlings grow, they continuously fine-tune the balance between plant growth and energy consumption for better plant fitness. Mitochondria are essential to generate energy. Here, Canal et al. generated single mutants for a gene involved in the mitochondrial respiratory chain – CYTOCHROME C-1 (CYTC-1), which caused defective mitochondrial energy production, membrane potential, lower ATP content, and a reduced growth rate in the cytc-1 mutants.  Some of the mutant phenotypes resemble those of plants with abnormal Target of Rapamycin (TOR) signaling. TOR is a protein that integrates growth-related processes in all eukaryotes. The authors showed that TOR activity is impaired in the cytc-1 mutants. In contrast, TOR overexpression rescued the seedling growth and low ATP level of cytc-1 mutant. The authors conclude that plants can coordinate their metabolism in response to the disruption of the mitochondrial function in the cytc-1 mutation, which anticipates energy exhaustion and  speculates that conditions by reducing TOR activity levels and slowing growth. This study also sheds light on how mitochondria communicate their status to the rest of the cell. (Summary by Yueh Cho @YuehCho1984) New Phytol. 10.1111/nph.19506.

Unveiling distinct responses of maize primary and seminal roots under drought stress

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Can you imagine going a day without a sip of water? Neither can plants. Water is essential for supporting diverse physiological processes in plants, including photosynthesis, nutrient transport, temperature regulation, and maintenance of cell turgidity. However, with global increase in temperature and shift in weather patterns, droughts have become increasingly frequent and prolonged that severely impact plant growth and productivity. Plants modulate their root system architecture to sustain their water acquisition capacity under drought stress. In this study, Protto et al investigated the growth pattern and hydraulic response of maize roots subjected to drought stress. Although growth inhibition and reduction in hydraulic conductivity was observed in both primary roots (PR) and seminal roots (SR) under stress conditions, SR were more sensitive to drought stress than PR. Moreover, relative abundance of aquaporins, involved in water transport across cell membranes, declined more in PR than SR under water deficit. Drought stress can also alter suberin and lignin deposition in the root layers, therefore, the authors examined the root anatomy. Suberin and lignin deposition was increased in PR endodermis but not in SR during water deficit. These findings clearly demonstrate distinct anatomical and hydraulic responses among various root types in maize. The unique functional characteristics and developmental plasticity of the maize root system may improve plant resilience in the face of drought stress. (Summary by Abira Sahu @AbiraSahu) Plant Physiol. 10.1093/plphys/kiad675

Auxin receptor OsTIR1 mediates auxin signaling during seed filling in rice

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Throughout the world, cereal endosperm is a major source of food. However, little is known about the molecular mechanisms underlying the import of sugar into the endosperm of rice plants (Oryza sativa) and how these pathways relate to auxin signaling. In this paper, Wu et al. investigate the role of auxin receptor OsTIR1 (Oryza sativa transport inhibitor response 1) in rice seed filling and its relationship with sugar import into the endosperm. The authors found that OsTIR1 mediates sugar import into endosperm via the auxin signaling component OsARF25 interacting with the sugar transporter OsSWEET11. Mutations in OsTIR1 repressed starch accumulation and reduced grain yield and quality, while overexpression of the gene improved starch accumulation and grain yield and quality. OsTIR1 has been shown to be highly expressed in the endosperm, nucellar projection, nucellar epidermis, aleurone layer cells, and ovular vascular trace, suggesting a possible route for sugar to enter the endosperm. The main auxin signaling element implicated in rice grain filling is known to be OsAR25, which interacts with the sugar transporter OsSWEET11. It has been hypothesized that OsIAA1 interacts directly with OsARF25 to influence OsTIR1-regulated endosperm development. Compared to wild-type plants, the overexpression of OsTIR1 improved grain quality and boosted grain output by 32% to 52% over the course of three years of field trials. Additionally, the authors observed that lower grain size and grain yield in tir1 mutant lines might also result from slender stems and less adventitious roots in tir1 mutant lines relative to wild-type plants. (Summary by Muhammad Aamir Khan @MAKNature1998) Plant Physiol. 10.1093/plphys/kiae013

Receptor-associated kinases control lipid provisioning in plant–fungal symbiosis

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Most plants benefit from symbiotic associations with fungi, in which the fungi aid in nutrient update particularly of phosphate, and the plant returns the favor by supplying the fungi with lipids. Several but not all of the molecular players required for these important pathways have been identified. Here Ivanov and Harrison have uncovered additional components, the membrane-bound CYCLIN-DEPENDENT KINASE-LIKE proteins CKL1 and CKL2. The genes encoding CKL1 and 2 are upregulated in fungal-colonized Medicago truncatula roots. CRISPR/Cas9 mutations show that the genes are required for successful colonization and arbuscule establishment. Expression of these genes activates downstream pathways required for production of the lipid reward, and this activity depends on CKL1 and 2 kinase activity, membrane-localization, and interaction with the leucine-rich repeat receptor-like kinase DMI2 and a subset of LysM receptor kinases. (Summary by Mary Williams @PlantTeaching) Science  10.1126/science.ade1124

Convergent evolution in pitcher plant traps reveals a mechanism for composite trait evolution

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It’s easy for most of us to grasp how an enzyme evolves new functions or substrate specificities, but envisioning how something incredibly complex like the human eye can be quite challenging (even Darwin was stumped). In this fascinating paper, Chomicki et al. asked how two geographically separated carnivorous pitcher plants evolved the same complex trap mechanism, which in part addresses this conundrum. Specifically, they looked at Nepenthes gracilis and Nepenthes pervillei, both of which use a springboard mechanism to trap insects. The trap requires three components, each useless without the other two: a horizontal lid that hovers above the pitcher, a slippery but not too-slippery surface on the underside of the lid, and a hinge on the lid that, when hit by rain, shakes the insects into the trap (see video). A phylogenetic analysis ruled out a single evolutionary origin for the trap mechanism, indicating that they are the product of convergent evolution. The three traits show independent evolution, indicating that the complex trait is a result of “spontaneous coincidence” in which the chance occurrence of the three traits provides a selective advantage that becomes fixed. This article is accompanied by another example of complex trait evolution (in snails) and a related perspective. (Summary by Mary Williams @PlantTeaching) Science 10.1126/science.ade0529. (Perspective article 10.1126/science.adm9239).

The global distribution of plant diversity and its significance to humans

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Plants shape ecosystems and sustain human life. Only a small portion of plant diversity is currently known to be in use, even though most plants may be useful to humans. Over time, certain species become widespread, but others are native to specific geographical regions. Thus, to manage plant resources efficiently and sustainably, people must understand the regional patterns of species variation. Pironon et al. followed Economic Botany Data Collection Standards to examine how 35,687 plant species are used worldwide for ten categories (food, materials, fuels, medicines, and others). All categories showed similar latitudinal variation in used plant species richness, representing greater values in the tropics but diminishing toward high latitudes. However, there are notable differences between temperate and tropical regions. Temperate environments contain more vertebrate food, social, and poisonous plant species. Tropical habitats have more species related to food, materials, and medicine. Human-used plants are more diverse in Mesoamerica, the Horn of Africa, and Southern Asia, but fewer protected areas in these locations reduce the biodiversity of exploited species. The relationship between species diversity and plant variety suggests safeguarding biodiversity hotspots protects these species. Multiple species and their genetic diversity are underrepresented in seed banks and botanical gardens. Therefore, it is crucial to identify and understand the diversity and geographic spread of plant species used by people to implement conservation policies and develop plant-derived solutions to global concerns like hunger, diseases, and climate change.  (Summary by Maneesh Lingwan @LingwanManeesh) Science 10.1126/science.adg8028

Nuclear pore and nucleoskeleton continuum

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Mermet et al. identify a protein that provides a continuum between the nucleoskeleton and the nuclear pore complex basket via short peptide motifs.

 https://doi.org/10.1093/plcell/koad236

 Christophe Tatout and Aline Probst

iGReD, Université Clermont Auvergne, CNRS, INSERM, 63001 Clermont-Ferrand, France

Background: The nuclear envelope is made up of a double membrane that separates the nucleus from the cytoplasm. It isolates and protects the DNA and creates two functional compartments with DNA replication and transcription taking place inside the nucleus and translation in the cytoplasmic compartment. The nuclear envelope is associated inside the nucleus with the nucleoskeleton, a nuclear structure composed of lamins and their associated proteins. The nuclear envelope is punctuated by thousands of nuclear pore complexes (NPCs) that not only regulate the trafficking of macromolecules into and out of the nucleus but also play significant roles in transcription regulation.

Question: To function in a coordinated manner, the nuclear envelope, NPCs and nucleoskeleton must be closely linked by a network of protein-protein interactions. These are poorly documented in plants as the plant-specific proteins within these structures have only recently been described. This motivated us to investigate the characteristics and functions of these interactions.

Findings: One such plant-specific protein is KAKU4, a component of the nucleoskeleton in which, using Arabidopsis as a model species, we identified three short peptide motifs of about 30 amino acids each. These motifs allow protein–protein interaction with the CRWN proteins, the main component of the plant nucleoskeleton and are required for elongation of the nucleus in differentiating tissues. The motifs were also found in NUP82 and NUP136, two plant-specific nucleoporins, suggesting that KAKU4 diverged from an ancestral nucleoporin, which had the ability to interact with the nucleoskeleton, and led to the emergence of KAKU4 as a new component of the plant nucleoskeleton.

Next steps: In future, it will be important to assess if the NPC–nucleoskeleton physical interactions identified are essential to anchor the nucleoskeleton at the nuclear envelope and to control NPC composition and distribution. Whether they regulate gene expression or chromatin organisation in response to stress should also be investigated.

Reference:

Sarah Mermet, Maxime Voisin, Joris Mordier, Tristan Dubos, Sylvie Tutois, Pierre Tuffery, Célia Baroux, Kentaro Tamura, Aline V. Probst, Emmanuel Vanrobays, Christophe Tatout. (2023). Evolutionarily conserved protein motifs drive interactions between the plant nucleoskeleton and nuclear pores. https://doi.org/10.1093/plcell/koad236

Autophagy regulation by HLS1-mediated acetylation

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Huang et al. explore the molecular mechanism underlying the regulation of autophagy by HLS1.

 https://doi.org/10.1093/plcell/koad252

 By Li Huang, Xing Wen, Lian Jin, Huihui Han, and Hongwei Guo

New Cornerstone Science Laboratory, Institute of Plant and Food Science, Department of Biology, School of Life Sciences, Southern University of Science and Technology (SUSTech); Shenzhen, Guangdong, 518055, China.

Background: Autophagy is a highly conserved process that delivers cytoplasmic components to the vacuole or lysosome for breakdown and recycling during stresses such as nutrient starvation. Almost every pivotal process of autophagy in yeast and mammals is regulated by an important post-translational modification (PTM) called protein acetylation. Nevertheless, whether and how core autophagy proteins in plants are regulated by acetylation remains elusive. HOOKLESS1 (HLS1) is a putative N-acetyltransferase, but its biochemical function has remained largely unclear. The loss-of-function mutant hls1-1 displays similar phenotypes to autophagy-defective (atg) mutants in senescence and immune responses, suggesting that there may be a relationship between HLS1 and plant autophagy.

Question: Is HLS1 involved in plant autophagy? Does HLS1 regulate autophagy? How does HLS1 function in autophagy?

Findings: We mainly uncovered the following four findings: (1) HLS1 is crucial for triggering autophagy during nutrient starvation in Arabidopsis (Arabidopsis thaliana); (2) HLS1 is a bona fide lysine acetyltransferase that can directly physically interact with and acetylate a key autophagy-related protein (ATG18a) in response to nutrient starvation; (3) HLS1-mediated ATG18a acetylation affects the ATG2-ATG18a interaction and the binding of ATG18a to phosphatidylinositol 3-phosphate to promote autophagy activation and plant responses to nutrient deprivation; and (4) the normal enzymatic activity of HLS1 is also important for apical hook development of etiolated seedlings, but HLS1-regulated autophagy by acetylating ATG18a is uncoupled from HLS1-mediated hook formation.

Next steps: We aim to explore how nutrient starvation modulates HLS1-mediated autophagy via ATG18a acetylation. Moreover, additional HLS1 substrates in multiple biological processes such as hook development are worthy of further investigation.

Reference:

Li Huang, Xing Wen, Lian Jin, Huihui Han, and Hongwei Guo. (2023). HOOKLESS1 acetylates AUTOPHAGY-RELATED PROTEIN18a to promote autophagy during nutrient starvation in Arabidopsis. https://doi.org/10.1093/plcell/koad252

Establishment of regeneration capability of callus cells

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Xu et al. demonstrate the transcriptional regulatory steps responsible for establishing the regenerating capability of callus during Arabidopsis regeneration.

 https://doi.org/10.1093/plcell/koad255

 By Chongyi Xu1, Pengjie Chang1,2, Shiqi Guo1,2, Xiaona Yang1,2, Xinchun Liu1,2, Baofeng Sui1,2, Dongxue Yu1,2, Wei Xin1,2, and Yuxin Hu1,3

1 Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, China National Botanical Garden, Beijing 100093, China.

2 University of Chinese Academy of Sciences, Beijing 100049, China.

3 National Center for Plant Gene Research, Beijing 100093, China.

 Background:  Plant cells retain a remarkable capacity to regenerate new organs or entire individuals in the real world and under tissue-culture conditions. A well-established in vitro plant regeneration procedure applicable for transgenic and biotechnological uses generally starts with the induction of pluripotent callus cells, which is required for subsequent de novo shoot or root regeneration. Recent studies in Arabidopsis (Arabidopsis thaliana) have revealed that auxin-induced ectopic activation of root stem cell factors within callus cells establishes the shoot-regenerating capability, and some auxin signaling components involved in root development, such as AUXIN RESPONSE FACTOR (ARFs) and their downstream transcription factors LATERAL ORGAN BOUNDARIES DOMAIN (LBD), play critical roles in directing callus formation. However, the molecular link between these auxin signaling components and activation of root stem cell factors during callus induction is missing.

Question: What are the factors responsible for activation of root stem cell factors to establish callus pluripotency in Arabidopsis for in vitro regeneration?

Findings: We identified the Arabidopsis transcription factors WRKY23 and bHLH041 as a transcriptional activator and repressor, respectively, of the expression of root stem cell genes during auxin-induced callus formation. Genetic and molecular evidence revealed that auxin-induced WRKY23 downstream of ARF7 and ARF19 directly activates the transcription of PLETHORA 3 (PLT3) and PLT7 and the downstream target genes of their encoded proteins PLT1, PLT2, and WUSCHEL-RELATED HOMEOBOX 5 (WOX5), while LBD induces the removal of bHLH041, alleviating the transcriptional repression of PLT1, PLT2, and WOX5. We also demonstrated that two transcriptional pathways synergize the shoot-regenerating capability of callus cells. These findings elucidate the transcriptional mechanism underlying callus pluripotency establishment, which links auxin signaling and cellular reprogramming during in vitro plant regeneration programs.

Next steps: It will be worth identifying the orthologs of WRKY23 and bHLH041 in crops and economically important plants and exploring whether such regulatory mechanisms are conserved, which would potentially boost regeneration-based transgene and gene editing in these species.

Reference:

Chongyi Xu, Pengjie Chang, Shiqi Guo, Xiaona Yang, Xinchun Liu, Baofeng Sui, Dongxue Yu, Wei Xin, Yuxin Hu (2023). Transcriptional activation by WRKY23 and derepression by removal of bHLH041 coordinately establish callus pluripotency in Arabidopsis regeneration. https://doi.org/10.1093/plcell/koad255