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Author: Gwendolyn K. Kirschner.
The Plant Journal (2024)
Excerpts: "Udvardi and Sonali Roy, a former post-doctoral fellow with Udvardi at the Noble Research Institute and now an assistant professor at Tennessee State University, together with a team of experts on legume rhizobial symbiosis from Oklahoma, Cambridge and Shanghai, analysed the role of GLVs for nodule development and positioning in more detail (Roy et al., 2024)."
"Transcriptional reporter expression in transgenic hairy roots showed that the expression of the five GLVs overlapped at sites of nodule initiation (Figure 1b). Out of these, MtGLV6, MtGLV9 and MtGLV10 were induced by short-term nitrogen deprivation stress, suggesting a role in early stages of symbiosis, such as the dedifferentiation of cortical cells or the regulation of early nodulin genes."
"The nitrogen-induced GLV10 peptide could integrate the nitrogen signal from the soil to adaptation of the root architecture. GLV10p treatment also led to more microcolonies and infection thread initiations. The authors hypothesise that the increase in infection might be a compensation for the reduction in nodule number: The plant initiates more infection threads to make an optimal number of nodules and derive sufficient nitrogen."
Authors: Isabel Cristina Vélez-Bermúdez and Wolfgang Schmidt.
Nature Plants (2024)
Summary: "The functions of a small family of non-secreted peptides, originally identified as critical communicators of the plant’s iron status, have expanded. The involvement of these effectors in disparate signalling cascades underlines the pivotal role peptides have in responses to the environment."
Authors: Sonali Roy, Ivone Torres-Jerez, Shulan Zhang, Wei Liu, Katharina Schiessl, Divya Jain, Clarissa Boschiero, Hee-Kyung Lee, Nicholas Krom, Patrick X. Zhao, Jeremy D. Murray, Giles E. D. Oldroyd, Wolf-Rüdiger Scheible and Michael Udvardi.
The Plant Journal (2024)
Significance Statement: Nodule positioning is an understudied trait, yet it determines the length of the root that can support nodule formation and consequently the total number of functional nodules formed. We identify genetic factors called GOLVEN peptides that alter nodule and lateral root positioning on the primary root along with several other traits including nodule organ initiation and root architecture.
Abstract: "The conservation of GOLVEN (GLV)/ROOT MERISTEM GROWTH FACTOR (RGF) peptide encoding genes across plant genomes capable of forming roots or root-like structures underscores their potential significance in the terrestrial adaptation of plants. This study investigates the function and role of GOLVEN peptide-coding genes in Medicago truncatula. Five out of fifteen GLV/RGF genes were notably upregulated during nodule organogenesis and were differentially responsive to nitrogen deficiency and auxin treatment. Specifically, the expression of MtGLV9 and MtGLV10 at nodule initiation sites was contingent upon the NODULE INCEPTION transcription factor. Overexpression of these five nodule-induced GLV genes in hairy roots of M. truncatula and application of their synthetic peptide analogues led to a decrease in nodule count by 25–50%. Uniquely, the GOLVEN10 peptide altered the positioning of the first formed lateral root and nodule on the primary root axis, an observation we term ‘noduletaxis’; this decreased the length of the lateral organ formation zone on roots. Histological section of roots treated with synthetic GOLVEN10 peptide revealed an increased cell number within the root cortical cell layers without a corresponding increase in cell length, leading to an elongation of the root likely introducing a spatiotemporal delay in organ formation. At the transcription level, the GOLVEN10 peptide suppressed expression of microtubule-related genes and exerted its effects by changing expression of a large subset of Auxin responsive genes. These findings advance our understanding of the molecular mechanisms by which GOLVEN peptides modulate root morphology, nodule ontogeny, and interactions with key transcriptional pathways."
Authors: Carole Laffont and Florian Frugier.
New Phytologist (2024)
Abstract: "C-terminally encoded peptides (CEP) signaling peptides are drivers of systemic pathways regulating nitrogen (N) acquisition in different plants, from Arabidopsis to legumes, depending on mineral N availability (e.g. nitrate) and on the whole plant N demand. Recent studies in the Medicago truncatula model legume revealed how root-produced CEP peptides control the root competence for endosymbiosis with N fixing rhizobia soil bacteria through the activity of the Compact Root Architecture 2 (CRA2) CEP receptor in shoots. Among CEP genes, MtCEP7 was shown to be tightly linked to nodulation, and the dynamic temporal regulation of its expression reflects the plant ability to maintain a different symbiotic root competence window depending on the symbiotic efficiency of the rhizobium strain, as well as to reinitiate a new window of root competence for nodulation."
Authors: Marios I. Valmas, Moritz Sexauer, Katharina Markmann and Daniela Tsikou.
Plants (2023)
Abstract: "Plants engage in symbiotic relationships with soil microorganisms to overcome nutrient limitations in their environment. Among the best studied endosymbiotic interactions in plants are those with arbuscular mycorrhizal (AM) fungi and N-fixing bacteria called rhizobia. The mechanisms regulating plant nutrient homeostasis and acquisition involve small mobile molecules such as peptides and micro RNAs (miRNAs). A large number of CLE (CLAVATA3/EMBRYO SURROUNDING REGION-RELATED) and CEP (C-TERMINALLY ENCODED PEPTIDE) peptide hormones as well as certain miRNAs have been reported to differentially respond to the availability of essential nutrients such as nitrogen (N) and phosphorus (P). Interestingly, a partially overlapping pool of these molecules is involved in plant responses to root colonization by rhizobia and AM fungi, as well as mineral nutrition. The crosstalk between root endosymbiosis and nutrient availability has been subject of intense investigations, and new insights in locally or systemically mobile molecules in nutrient- as well as symbiosis-related signaling continue to arise. Focusing on the key roles of peptides and miRNAs, we review the mechanisms that shape plant responses to nutrient limitation and regulate the establishment of symbiotic associations with beneficial soil microorganisms."
Authors: Sonali Roy, Ivone Torres-Jerez, Shulan Zhang, Wei Liu, Katharina Schiessl, Clarissa Boschiero, Hee-Kyung Lee, Patrick X. Zhao, Jeremy D. Murray, Giles E. D. Oldroyd, Wolf-Rüdiger Scheible and Michael Udvardi.
bioRxiv (2022)
Abstract: "GLV/RGF peptide encoding genes can be identified in genomes of all plants that can form roots or root-like structures suggesting they were essential for transition of plants to land. In Medicago truncatula, five of fifteen GOLVEN(GLV)/ROOT MERISTEM GROWTH FACTOR (RGF) peptide coding genes were induced during nodule organogenesis and to a varying extent under nitrogen deficiency and auxin treatment. Expression of MtGLV9 and MtGLV10 at nodule initiation sites was dependent on the transcription factor NODULE INCEPTION. Overexpression of all five nodule-induced GLV genes in M. truncatula hairy roots as well as application of the corresponding synthetic peptides resulted in a 25-50% reduction in nodule number indicating GOLVENs are negative regulators of nodule organogenesis. The peptide GOLVEN10 shifted the position of the first formed lateral root (rhizotaxis) as well as the first formed nodule along the longitudinal primary root axis, a phenomenon we term (nodulotaxis), thereby reducing the absolute length of the zone of lateral organ formation on roots. Application of synthetic GOLVEN10 peptide caused an increase in cell number but not cell length in each root cortical cell layer causing an increase in root length and a consequent spatiotemporal delay in formation of the first lateral organ."
Authors: Candice H. Jones, April H. Hastwell, Peter M. Gresshoff and Brett J. Ferguson.
Chapter 6 in: Advances in Botanical Research, Vol. 102 (2022)
Abstract: "Plants coordinate development through complex signaling networks involving many different types of molecules, genes, proteins, and hormones. CLAVATA3-Endosperm Surrounding Region-related (CLE) peptides are one such family of signaling molecules that have roles in general plant development as well during interactions with abiotic and biotic factors. Members of the CLE peptide family have been well studied in the model species, Arabidopsis thaliana; with extensive CLV3, CLE40 and TDIF signaling pathways having been identified. These CLE peptide pathways tend to have three core elements including a CLE peptide, which is perceived by a Receptor-Kinase that regulates a WUSCHEL-like homeobox transcription factor. Such elements are also present in the Autoregulation of Nodulation pathway that controls nodule number during the legume-rhizobia symbiosis. In the soybean genome, 84 CLE peptide-encoding genes are present, although little research outside of nodulation has been undertaken to understand how they modulate growth in the model legume. Understanding CLE peptides may provide novel targets to improve soybean growth and productivity. Moreover, it also represents a unique opportunity to study CLE peptides in the context of beneficial symbiosis with rhizobia and mycorrhizae of which A. thaliana cannot undergo. This chapter reviews the current understanding of CLE peptide signaling in plants, what is currently known about soybean orthologues, and avenues that we can target to improve soybean development using the CLE peptides and their associated molecular networks."
Authors: Maria Lebedeva, Mahboobeh Azarakhsh, Darina Sadikova and Lyudmila Lutova.
Plants (2021)
Abstract: "The interaction between legume plants and soil bacteria rhizobia results in the formation of new organs on the plant roots, symbiotic nodules, where rhizobia fix atmospheric nitrogen. Symbiotic nodules represent a perfect model to trace how the pre-existing regulatory pathways have been recruited and modified to control the development of evolutionary “new” organs. In particular, genes involved in the early stages of lateral root development have been co-opted to regulate nodule development. Other regulatory pathways, including the players of the KNOX-cytokinin module, the homologues of the miR172-AP2 module, and the players of the systemic response to nutrient availability, have also been recruited to a unique regulatory program effectively governing symbiotic nodule development. The role of the NIN transcription factor in the recruitment of such regulatory modules to nodulation is discussed in more details."
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Authors: Mengdi Fu, Xiaolei Yao, Xiaolin Li, Jing Liu, Mengyan Bai, Zijun Fang, Jiming Gong, Yuefeng Guan and Fang Xie.
The Plant Journal (2024)
Significance Statement: GmNLP1 and GmNLP4 activate nitrate-induced CLE peptides NIC1a/b to mediate nitrate-regulated root nodulation.
Abstract: "Symbiotic nitrogen fixation is an energy-intensive process, to maintain the balance between growth and nitrogen fixation, high concentrations of nitrate inhibit root nodulation. However, the precise mechanism underlying the nitrate inhibition of nodulation in soybean remains elusive. In this study, CRISPR-Cas9-mediated knockout of GmNLP1 and GmNLP4 unveiled a notable nitrate-tolerant nodulation phenotype. GmNLP1b and GmNLP4a play a significant role in the nitrate-triggered inhibition of nodulation, as the expression of nitrate-responsive genes was largely suppressed in Gmnlp1b and Gmnlp4a mutants. Furthermore, we demonstrated that GmNLP1b and GmNLP4a can bind to the promoters of GmNIC1a and GmNIC1b and activate their expression. Manipulations targeting GmNIC1a and GmNIC1b through knockdown or overexpression strategies resulted in either increased or decreased nodule number in response to nitrate. Additionally, transgenic roots that constitutively express GmNIC1a or GmNIC1b rely on both NARK and hydroxyproline O-arabinosyltransferase RDN1 to prevent the inhibitory effects imposed by nitrate on nodulation. In conclusion, this study highlights the crucial role of the GmNLP1/4-GmNIC1a/b module in mediating high nitrate-induced inhibition of nodulation."
Authors: María Isabel Puga, César Poza-Carrión, Iris Martinez-Hevia, Laura Perez-Liens and Javier Paz-Ares
Journal of Plant Research (2024)
Abstract: "Phosphorus is indispensable for plant growth and development, with its status crucial for determining crop productivity. Plants have evolved various biochemical, morphological, and developmental responses to thrive under conditions of low P availability, as inorganic phosphate (Pi), the primary form of P uptake, is often insoluble in soils. Over the past 25 years, extensive research has focused on understanding these responses, collectively forming the Pi starvation response system. This effort has not only expanded our knowledge of strategies to cope with Pi starvation (PS) but also confirmed their adaptive significance. Moreover, it has identified and characterized numerous components of the intricate regulatory network governing P homeostasis. This review emphasizes recent advances in PS signaling, particularly highlighting the physiological importance of local PS signaling in inhibiting primary root growth and uncovering the role of TORC1 signaling in this process. Additionally, advancements in understanding shoot-root Pi allocation and a novel technique for studying Pi distribution in plants are discussed. Furthermore, emerging data on the regulation of plant-microorganism interactions by the PS regulatory system, crosstalk between the signaling pathways of phosphate starvation, phytohormones and immunity, and recent studies on natural variation in Pi homeostasis are addressed.
Authors: Momoyo Ito, Yuri Tajima, Mari Ogawa-Ohnishi, Hanna Nishida, Shohei Nosaki, Momona Noda, Naoyuki Sotta, Kensuke Kawade, Takehiro Kamiya, Toru Fujiwara, Yoshikatsu Matsubayashi and Takuya Suzaki.
Nature Communications (2024)
Editors view: The authors show IRON MAN peptides have an essential role in symbiotic nitrogen fixation during legume-rhizobium symbiosis. The peptides additionally function to regulate nitrogen homeostasis by controlling nitrogen-iron balance.
Abstract: "Legumes control root nodule symbiosis (RNS) in response to environmental nitrogen availability. Despite the recent understanding of the molecular basis of external nitrate-mediated control of RNS, it remains mostly elusive how plants regulate physiological processes depending on internal nitrogen status. In addition, iron (Fe) acts as an essential element that enables symbiotic nitrogen fixation; however, the mechanism of Fe accumulation in nodules is poorly understood. Here, we focus on the transcriptome in response to internal nitrogen status during RNS in Lotus japonicus and identify that IRON MAN (IMA) peptide genes are expressed during symbiotic nitrogen fixation. We show that LjIMA1 and LjIMA2 expressed in the shoot and root play systemic and local roles in concentrating internal Fe to the nodule. Furthermore, IMA peptides have conserved roles in regulating nitrogen homeostasis by adjusting nitrogen-Fe balance in L. japonicus and Arabidopsis thaliana. These findings indicate that IMA-mediated Fe provision plays an essential role in regulating nitrogen-related physiological processes."
Authors: Michael Taleski, Marvin Jin, Kelly Chapman, Katia Taylor, Courtney Winning, Manuel Frank, Nijat Imin and Michael A. Djordjevic.
Journal of Experimental Botany (2024)
Abstract: "A growing understanding is emerging of the roles of peptide hormones in local- and long-distance signalling that coordinates plant growth and development as well as responses to the environment. C-TERMINALLY ENCODED PEPTIDE (CEP) signalling triggered by its interaction with CEP RECEPTOR 1 (CEPR1) is known to play roles in systemic nitrogen (N)-demand signalling, legume nodulation, and root system architecture. Recent research provides further insight into how CEP signalling operates, which involves diverse downstream targets and interactions with other hormone pathways. Additionally, there is emerging evidence of CEP signalling playing roles in N-allocation, root responses to carbon levels, the uptake of other soil nutrients such as phosphorus and sulphur, root responses to arbuscular mycorrhizal fungi, plant immunity, and reproductive development. These findings suggest CEP signalling more broadly coordinates growth across the whole plant in response to diverse environmental cues. Moreover, CEP signalling and function appears to be conserved in angiosperms. In this manuscript, we review the recent advances in CEP biology with a focus on soil nutrient uptake, root system architecture and organogenesis, and roles in plant-microbe interactions. Furthermore, we address knowledge gaps and future directions in this research field."
Authors: Qi Di, Yi Li, Danping Zhang, Wei Wu, Lin Zhang, Xing Zhao, Li Luo and Liangliang Yu.
Plant Signaling & Behavior (2022)
Abstract: "Phytosulfokines (PSKs) are a class of tyrosine-sulfated pentapeptides. PSK-α, PSK-γ, and PSK-δ are three reported PSK members involved in regulating plant growth, development, and resistance to biotic and abiotic stresses. Here, we reported a novel type of PSK, PSK-ε with the sequence YSO3VYSO3TN, and its precursor proteins (MtPSKε, LjPSKε, and GmPSKε), specifically from legume species. PSK-ε peptide differs from PSK-δ by one amino acid and is close to PSK-δ in the phylogenetic relationship. Expression profile analysis showed that MtPSKε was highly expressed in Medicago truncatula roots, especially in root tips and emerged lateral roots. Application of the synthetic sulfated PSK-ε peptide and overexpression of MtPSKε significantly promoted M. truncatula root elongation and increased lateral root number, probably by inducing cell division and expansion in roots. Furthermore, MtPSKε expression was induced by rhizobia infection and was detected in root nodules including nodule primordia. Both PSK-ε peptide treatment and MtPSKε overexpression significantly increased nodule number in M. truncatula. Taken together, these results demonstrate that PSK-ε, a novel type of phytosulfokine, positively regulates root elongation and formation of lateral root and root nodule in M. truncatula."
Authors: Yu-Heng Hsieh, Yi-Hsien Wei, Jui-Chi Lo, Hsuan-Yu Pan and Shu-Yi Yang.
New Phytologist (2022)
Abstract: "Plant lateral root (LR) growth is usually stimulated by arbuscular mycorrhizal (AM) symbiosis. However, the molecular mechanism is still unclear. We used gene expression analysis, peptide treatment and virus-induced gene alteration assays to demonstrate that C-terminally encoded peptide (CEP2) expression in tomato was downregulated during AM symbiosis to mitigate its negative effect on LR formation through an auxin-related pathway. We showed that enhanced LR density and downregulated CEP2 expression were observed during mycorrhizal symbiosis. Synthetic CEP2 peptide treatment reduced LR density and impaired the expression of genes involved in indole-3-butyric acid (IBA, the precursor of indole-3-acetic acid (IAA)) to IAA conversion, auxin polar transport and the LR-related signaling pathway; however, application of IBA or synthetic auxin NAA to the roots may rescue both defective LR formation and reduced gene expression. CEP receptor 1 (CEPR1) might be the receptor of CEP2 since its knockdown plants did not respond to CEP2 treatment. Most importantly, the LR density of CEP2 overexpression or knockdown plants could not be further increased by AM inoculation, suggesting that CEP2 was critical for AM-induced LR formation. These results indicated that AM symbiosis may regulate root development by modulating CEP2, which affects the auxin-related pathway."
Authors: Sonali Roy and Lena Maria Müller.
Trends in Plant Science (2022)
Highlights: Plant interactions with arbuscular mycorrhizal fungi, beneficial soil bacteria, and nutrient homeostasis are optimized by an interconnected network of peptide signals. Symbiosis-regulating signaling peptides are members of large protein families, often with a variety of functions in plant physiology and development. The mechanism of peptide-signaling specificity in the context of plant–microbe interactions, nutrient homeostasis, and cross-kingdom peptide mimicry involves antagonism and coordination between individual peptide signals. Although many of the symbiosis-associated peptide signaling pathways converge at common downstream signaling hubs and intersect with phytohormone signaling, the signaling outcomes are, at least partially, unique.
Abstract: "Plants engage in mutually beneficial relationships with microbes, such as arbuscular mycorrhizal fungi or nitrogen-fixing rhizobia, for optimized nutrient acquisition. In return, the microbial symbionts receive photosynthetic carbon from the plant. Both symbioses are regulated by the plant nutrient status, indicating the existence of signaling pathways that allow the host to fine-tune its interactions with the beneficial microbes depending on its nutrient requirements. Peptide hormones coordinate a plethora of developmental and physiological processes and, recently, various peptide families have gained special attention as systemic and local regulators of plant–microbe interactions and nutrient homeostasis. In this review, we identify five ‘rules’ or guiding principles that govern peptide function during symbiotic plant–microbe interactions, and highlight possible points of integration with nutrient acquisition pathways."
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