Plant Physiology

Pullagurla, Naga Jyothi; Shome, Supritam; Liu, Guizhen; Jessen, Henning J; Laha, Debabrata

2024 Plant Physiology

doi: 10.1093/plphys/kiae454pmid: 39190827

Land plants have evolved sophisticated sensing mechanisms and signaling pathways to adapt to phosphate-limited environments. While molecular players contributing to these adaptations in flowering plants have been described, how nonvascular bryophytes regulate phosphate (Pi) homeostasis remained largely unknown. In this study, we present findings that both male and female plants of the liverwort Marchantia polymorpha respond to altered phosphate availability through substantial developmental changes. We show that the second messenger inositol pyrophosphates (PP-InsPs) respond more quickly to changes in cellular Pi status than the lower inositol phosphates, highlighting a functional relationship between PP-InsP and Pi homeostasis in M. polymorpha. To further corroborate the possible involvement of PP-InsP in Pi homeostasis, we characterized M. polymorpha INOSITOL (1,3,4) TRIPHOSPHATE 5/6 KINASE1 (MpITPK1) that phosphorylates InsP6 to generate InsP7 both in vitro and in vivo. Consistent with the role of PP-InsPs in Pi homeostasis, M. polymorpha lines with enhanced MpITPK1 expression leading to the accumulation of 5-InsP7 and an InsP8 isomer, exhibit altered expression of phosphate starvation induced (PSI) genes and display attenuated responses to low phosphate. The characterization of MpPHO1-deficient plants with dramatically increased levels of 1,5-InsP8 further supports the role of PP-InsP in Pi homeostasis in this liverwort species. Notably, our study unveiled that MpITPK1 rescues the deregulated Pi homeostasis in Arabidopsis (Arabidopsis thaliana) ITPK1-deficient plants, suggesting that liverwort and eudicots share a functional ITPK1 homolog. In summary, our study provides insights into the regulation of Pi homeostasis by ITPK1-derived PP-InsPs in M. polymorpha.

Bates, Philip D; Shockey, Jay

2024 Plant Physiology

doi: 10.1093/plphys/kiae658pmid: 39657632

Plant lipids represent a fascinating field of scientific study, in part due to a stark dichotomy in the limited fatty acid (FA) composition of cellular membrane lipids vs the huge diversity of FAs that can accumulate in triacylglycerols (TAGs), the main component of seed storage oils. With few exceptions, the strict chemical, structural, and biophysical roles imposed on membrane lipids since the dawn of life have constrained their FA composition to predominantly lengths of 16–18 carbons and containing 0–3 methylene-interrupted carbon-carbon double bonds in cis-configuration. However, over 450 “unusual” FA structures can be found in seed oils of different plants, and we are just beginning to understand the metabolic mechanisms required to produce and maintain this dichotomy. Here we review the current state of plant lipid research, specifically addressing the knowledge gaps in membrane and storage lipid synthesis from 3 angles: pathway fluxes including newly discovered TAG remodeling, key acyltransferase substrate selectivities, and the possible roles of “metabolons.”

Lung, Shiu-Cheung; Chye, Mee-Len

2024 Plant Physiology

doi: 10.1093/plphys/kiae565pmid: 39431550

While lipids serve as important energy reserves, metabolites, and cellular constituents in all forms of life, these macromolecules also function as unique carriers of information in plant communication given their diverse chemical structures. The signal transduction process involves a sophisticated interplay between messengers, receptors, signal transducers, and downstream effectors. Over the years, an array of plant signaling proteins have been identified for their crucial roles in perceiving lipid signals. However, the mechanistic effects of lipid binding on protein functions remain largely elusive. Recent literature has presented numerous fascinating models that illustrate the significance of protein–lipid interactions in mediating signaling responses. This review focuses on the category of lipophilic signaling proteins that encompass a hydrophobic binding pocket located outside of cellular membranes and provides an update on the lessons learned from two of these structures, namely the acyl-CoA–binding and steroidogenic acute regulatory protein-related lipid transfer domains. It begins with a brief overview of the latest advances in understanding the functions of the two protein families in plant communication. The second part highlights five functional mechanisms of lipid ligands in concert with their target signaling proteins.

Zhang, Tianen; Zhu, Jingjuan; Liu, Yang; Pei, Yanfei; Pei, Yayue; Wei, Zhenzhen; Miao, Pengfei; Peng, Jun; Li, Fuguang; Wang, Zhi

2024 Plant Physiology

doi: 10.1093/plphys/kiae618pmid: 39560107

Light signaling plays a substantial role in regulating plant development, including the differentiation and elongation of single-celled tissue. However, the identity of the regulatory machine that affects light signaling on root hair cell (RHC) development remains unclear. Here, we investigated how darkness inhibits differentiation and elongation of RHC in Arabidopsis (Arabidopsis thaliana). We found that light promotes the growth and development of RHC. RNA-seq analysis showed that light signaling regulates the differentiation of RHC by promoting the expression of specific genes in the root epidermis associated with cell wall remodeling, jasmonic acid, auxin, and ethylene signaling pathways. Together, these genes integrate light and phytohormone signals with root hair (RH) development. Our investigation also revealed that the core light signal factor ELONGATED HYPOCOTYL 5 (HY5) directly interacts with the key RH development factor ROOT HAIR DEFECTIVE6 (RHD6), which promotes the transcription of RSL4. However, CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) repressed the RHD6 function through the COP1–HY5 complex. Our genetic studies confirm associations between RHD6, HY5, and COP1, indicating that RHD6 largely depends on HY5 for RH development. Ultimately, our work suggests a central COP1–HY5–RHD6 regulatory module that integrates light signaling and RH development with several downstream pathways, offering perspectives to decipher single-celled RH development.

Cheng, Jintao; Wen, Suying; Li, Kexin; Zhou, Yixuan; Zhu, Mengtian; Neuhaus, H Ekkehard; Bie, Zhilong

2024 Plant Physiology

doi: 10.1093/plphys/kiae597pmid: 39679528

Hexoses are essential for plant growth and fruit development. However, the precise roles of hexose/H+ symporters in postphloem sugar transport and cellular sugar homeostasis in rapidly growing fruits remain elusive. To elucidate the functions of hexose/H+ symporters in cucumber (Cucumis sativus L.) fruits, we conducted comprehensive analyses of their tissue-specific expression, localization, transport characteristics, and physiological functions. Our results demonstrate that CsHT3 (C. sativus hexose transporter), CsHT12, and CsHT16 are the primary hexose/H+ symporters expressed in cucumber fruits. CsHT3 and CsHT16 are localized in the sieve element–companion cell during the ovary and early fruit development stages. As the fruit develops and expands, the expression of both symporters shifts to phloem parenchyma cells. The CsHT16 knockout mutant produces shorter fruits with a larger circumference, likely due to impaired sugar and phytohormone homeostasis. Concurrent reduction of CsHT3, CsHT12, and CsHT16 expression leads to decreased fruit size. Conversely, CsHT3 overexpression results in increased fruit size and higher fruit sugar levels. These findings suggest that CsHT16 plays an important role in maintaining sugar homeostasis, which shapes the fruit, while CsHT3, CsHT12, and CsHT16 collectively regulate the supply of carbohydrates required for cucumber fruit enlargement.

Pandey, Mandavi; Verma, Lokesh; Kohli, Pawandeep Singh; Singh, Bhagat; Kochi, Abhijith; Giri, Jitender

2024 Plant Physiology

doi: 10.1093/plphys/kiae453pmid: 39190806

Plants require phosphate (Pi) for proper growth and development but often face scarcity of this vital nutrient in the soil. Pi starvation triggers membrane lipid remodeling to utilize the membrane phospholipid-bound Pi in plants. In this process, phospholipids are replaced by non-Pi-containing galactolipids (monogalactosyldiacylglycerol, MGDG; digalactosyldiacylglycerol, DGDG) and sulfolipids. The galactolipids ratio (MGDG:DGDG) is suggested to influence jasmonic acid (JA) biosynthesis. However, how the MGDG:DGDG ratio, JA levels, and root growth are coordinated under Pi deficiency in rice (Oryza sativa) remains unknown. Here, we characterized DGDG synthase 1 (OsDGD1) for its role in regulating root development by maintaining metabolic flux for JA biosynthesis. We showed that OsDGD1 is responsive under low Pi and is under the direct control of Phosphate Starvation Response 2, the master regulator of low Pi adaptations. Further, OsDGD1 knockout (KO) lines showed marked phenotypic differences compared to the wild type, including a significant reduction in root length and biomass, leading to reduced Pi uptake. Further, lipidome analyses revealed reduced DGDG levels in the KO line, leading to reduced membrane remodeling, thus affecting P utilization efficiency. We also observed an increase in the MGDG:DGDG ratio in KO lines, which enhanced the endogenous JA levels and signaling. This imbalance of JA in KO plants led to changes in auxin levels, causing drastic root growth inhibition. These findings indicate the critical role of OsDGD1 in maintaining optimum levels of JA during Pi deficiency for conducive root growth. Besides acting as signaling molecules and structural components, our study widens the role of lipids as metabolic flux controllers for phytohormone biosynthesis.

Zhu, Jin-dong; Liang, Yu-ping; Yan, Hong-ru; Wu, Qi-qi; Zhang, Yue-yue; Zhou, Fang-yuan; Zhang, Xiao; Zhao, Xiang

2024 Plant Physiology

doi: 10.1093/plphys/kiae537pmid: 39365781

NONPHOTOTROPIC HYPOCOTYL3 (NPH3) is a key regulator of hypocotyl phototropism under both low- and high-intensity blue light (LBL/HBL), mediating phototropin1 (phot1) and phot2 signaling. NPH3 undergoes dephosphorylation and is released from the plasma membrane (PM) upon blue light irradiation. However, how its phosphorylation status and PM localization mediate phot1 and phot2 signaling in Arabidopsis (Arabidopsis thaliana) remains elusive. In this study, we found that fusing NPH3 with GFP at its C-terminus (N3G) impaired its release from the PM, a defect exacerbated by a phosphorylation-deficient mutation, resulting in a dephosphorylated NPH3-GFP (N3AG). Unlike N3G, transgenic lines expressing N3AG exhibited defective hypocotyl phototropism under HBL, which could be rescued by myristoylation at the N-terminus of N3AG (mN3AG), indicating that NPH3 phosphorylation is not essential for HBL-induced phototropic responses when it is artificially anchored at the PM via its N-terminus. Furthermore, genetic analysis revealed that N3AG anchored to the PM by its N-terminus (as in mN3AG) only rescues phot1-mediated HBL responses, which require RPT2. However, N3AG failed to regulate phot2-mediated HBL signaling, regardless of its PM orientation. Taken together, our results revealed that NPH3 phosphorylation is essential for phot2-mediated hypocotyl phototropism under HBL, but is not required for phot1-mediated HBL signaling when the NPH3 N-terminus is PM-anchored.

Cai, Yingqi; Horn, Patrick J

2024 Plant Physiology

doi: 10.1093/plphys/kiae533pmid: 39566075

Plant neutral lipids, also known as “vegetable oils”, are synthesized within the endoplasmic reticulum (ER) membrane and packaged into subcellular compartments called lipid droplets (LDs) for stable storage in the cytoplasm. The biogenesis, modulation, and degradation of cytoplasmic LDs in plant cells are orchestrated by a variety of proteins localized to the ER, LDs, and peroxisomes. Recent studies of these LD-related proteins have greatly advanced our understanding of LDs not only as steady oil depots in seeds but also as dynamic cell organelles involved in numerous physiological processes in different tissues and developmental stages of plants. In the past 2 decades, technology advances in proteomics, transcriptomics, genome sequencing, cellular imaging and protein structural modeling have markedly expanded the inventory of LD-related proteins, provided unprecedented structural and functional insights into the protein machinery modulating LDs in plant cells, and shed new light on the functions of LDs in nonseed plant tissues as well as in unicellular algae. Here, we review critical advances in revealing new LD proteins in various plant tissues, point out structural and mechanistic insights into key proteins in LD biogenesis and dynamic modulation, and discuss future perspectives on bridging our knowledge gaps in plant LD biology.

Trontin, Jean-François; Sow, Mamadou Dia; Delaunay, Alain; Modesto, Ines; Teyssier, Caroline; Reymond, Isabelle; Canlet, Francis; Boizot, Nathalie; Le Metté, Claire; Gibert, Audrey; Chaparro, Cristian; Daviaud, Christian; Tost, Jörg; Miguel, Celia; Lelu-Walter, Marie-Anne; Maury, Stéphane

2024 Plant Physiology

doi: 10.1093/plphys/kiae600pmid: 39511700

Embryogenesis is a brief but potentially critical phase in the life cycle of a tree for adaptive phenotypic plasticity. Using somatic embryogenesis in maritime pine (Pinus pinaster Ait.), we found that temperature during the maturation phase affects embryo development and postembryonic tree growth for up to 3 yr. We examined whether this somatic stress memory could stem from temperature- and/or development-induced changes in DNA methylation. For this, we developed a 200 mb custom sequence capture bisulfite analysis of genes and promoters to identify differentially methylated cytosines (DMCs) between temperature treatments (18, 23, and 28 °C) and developmental stages (immature and cotyledonary embryos, shoot apical meristem of 2-yr-old plants) and investigate if these differences can be mitotically transmitted from embryonic to postembryonic development (epigenetic memory). We revealed a high prevalence of temperature-induced DMCs in genes (8% to 14%) compared to promoters (<1%) in all 3 cytosine contexts. Developmental DMCs showed a comparable pattern but only in the CG context and with a strong trend toward hypomethylation, particularly in the promoters. A high percentage of DMCs induced by developmental transitions were found memorized in genes (up to 45%–50%) and promoters (up to 90%). By contrast, temperature-induced memory was lower and confined to genes after both embryonic (up to 14%) and postembryonic development (up to 8%). Using stringent criteria, we identified 10 genes involved in defense responses and adaptation, embryo development, and chromatin regulation that are candidates for the establishment of a persistent epigenetic memory of temperature sensed during embryo maturation in maritime pine. Here, we provide evidence that DNA methylation marks established during the embryonic phase are transmitted to the postembryonic plant development phase.

Yang, Mingming; Du, Changhuan; Li, Meng; Wang, Yuanzhuo; Bao, Gege; Huang, Jinxiu; Zhang, Qingyan; Zhang, Shuzhen; Xu, Pengfei; Teng, Weili; Li, Qingqing; Liu, Shanshan; Song, Bo; Yang, Qiang; Wang, Zhikun

2024 Plant Physiology

doi: 10.1093/plphys/kiae485pmid: 39268876

Soybean (Glycine max [L.] Merr.) is a major oil-producing crop worldwide. Although several related proteins regulating soybean oil accumulation have been reported, little is known about the regulatory mechanisms. In this study, we characterized vascular plant one-zinc-finger 1A (GmVOZ1A) that interacts with WRINKLED 1a (GmWRI1a) using yeast 2-hybrid library screening. The GmVOZ1A–GmWRI1a interaction was further verified by protein–protein interaction assays in vivo and in vitro. GmVOZ1A enhanced the seed fatty acid and oil contents by regulating genes involved in lipid biosynthesis. Conversely, a loss-of-function mutation in GmVOZ1A resulted in a reduction in triacylglycerol (TAG) content in soybean. Protein–DNA interaction assays revealed that GmVOZ1A and GmWRI1a cooperate to upregulate the expression level of acyl-coenzyme A-binding protein 6a (GmACBP6a) and promote the accumulation of TAG. In addition, GmACBP6a overexpression promoted seed fatty acid and oil contents, as well as increased seed size and 100-seed weight. Taken together, these findings indicate that the transcription factor GmVOZ1A regulates soybean oil synthesis and cooperates with GmWRI1a to upregulate GmACBP6a expression and oil biosynthesis in soybean. The results lay a foundation for a comprehensive understanding of the regulatory mechanisms underlying soybean oil biosynthesis and will contribute to improving soybean oil production through molecular breeding approaches.