Antagonistic interactions between CLAVATA receptors shape maize ear development
Authors: Penelope L. Lindsay, Fang Xu, Lei Liu, Panagiotis Boumpas, Andres Reyes, Byoung‐Il Je, Mari Ogawa‐Ohnishi, Jarrett Man, Tara Skopelitis, Yoshikatsu Matsubayashi, Madelaine Bartlett, Shou‐Ling Xu, David Jackson
Venue: New Phytologist
Published: 2026
Summary Meristem activity is controlled by the CLAVATA (CLV) signaling pathway, which involves a suite of leucine‐rich receptor (LRR) receptors, receptor‐like proteins, and CLV‐EMBRYO SURROUNDING REGION (CLE) peptide ligands. FASCIATED EAR 3 (FEA3) is a leucine‐rich receptor (LRR) receptor‐like protein important for meristem maintenance in maize and acts independently of canonical CLV receptors. To identify FEA3's interaction network, we used TurboID‐based proximity labeling in Zea mays meristems and identified a putative co‐receptor, BARELY ANY MERISTEM 1D (BAM1D). BAM1D and FEA3 proximity labeling proteomes shared over 40 proteins, including many signaling proteins, suggesting they feed into a common signaling pathway. fea3 was epistatic to bam1d in the control of inflorescence meristem (IM) size, supporting the idea that FEA3 and BAM1D interact physically. However, fea3 and bam1d act antagonistically because fea3 mutants had larger IMs, whereas bam1d mutants produced smaller IMs. This study demonstrates how in vivo TurboID‐based proximity labeling clarifies complex genetic interactions between CLV receptors and expands our knowledge of downstream signaling components of CLV signaling pathways, which are largely uncharacterized. Our findings support the notion that multiple, partially overlapping CLV receptor complexes coordinately control meristem maintenance.
View Publication(DOI: 10.1111/nph.70950)Ontogenetic and time-course transcriptomic analyses of maize leaf primordia reveal regulators of transverse vein development
Authors: Maria Camila Medina, Lander Geadelmann, Diana Ruggiero, Erica Unger-Wallace, Erik Vollbrecht, Penelope L Lindsay, Samuel Leiboff
Venue: bioRxiv (preprint)
Published: 2026
Leaf vein patterning varies greatly among land plants and is linked to leaf structure and function. C4 plants, such as maize, have a denser arrangement of veins than C3 plants, which is hypothesized to be a pre-adaptive trait for C4 photosynthesis. Therefore, understanding how leaf veins are patterned has implications for maximizing photosynthetic efficiency. Major maize leaf veins, called longitudinal veins, are arranged in parallel and are interconnected by transverse veins. Recent work has established molecular factors controlling longitudinal vein development; however, it is unknown how transverse veins are patterned. Here, we investigated how transverse veins establish connections within the maize vascular network. We performed anatomical analyses of transverse veins and found that despite asynchronous development, transverse veins fully integrate into the longitudinal vein network. Tracing the ontogeny of transverse vein development using the marker PIN1a-YFP, we found that two sets of two initial cells on opposing sides of adjacent longitudinal veins recruit intervening ground cells to form the provascular strand. Treatment with auxin inhibitors did not abolish transverse vein initiation, suggesting an auxin-independent pre-pattern for transverse vein initiation. Through time-course RNAseq of leaf primordia, we identified a transcriptional signature that precedes transverse vein development. Two genes that belong to this gene cluster, EREB41 and EREB114, are necessary for transverse vein formation. Together, our studies establish the ontogeny of maize transverse vein development and reveal how new vascular connections are specified, assembled, and integrated into an existing vascular network.
View Publication(DOI: 10.64898/2026.10.28.761427)The pseudokinase CORYNE modulates Medicago truncatula inflorescence meristem branching and plays a conserved role in the regulation of arbuscular mycorrhizal symbiosis
Authors: Johnathan Orosz, Erica Xinlei Lin, Yerisf C Torres Ascurra, Mikayla Kappes, Penelope Lindsay, Sagar Bashyal, Hasani Everett, Chandan Kumar Gautam, David Jackson, Lena Maria Müller
Venue: Journal of Experimental Botany
Published: 2025
Abstract The CLAVATA signaling pathway regulates plant development and plant–environment interactions. CLAVATA signaling consists of mobile, cell-type or environment-specific CLAVATA3/ESR-related (CLE) peptides, which are perceived by a receptor complex consisting of leucine-rich repeat receptor-like kinases such as CLAVATA1 and receptor-like proteins such as CLAVATA2, which often functions with the pseudokinase CORYNE (CRN). CLAVATA signaling has been extensively studied in various plant species for its developmental role in meristem maintenance. In addition, CLAVATA signaling was implicated in plant–microbe interactions, including root nodule symbiosis and plant interactions with mutualistic arbuscular mycorrhizal (AM) fungi. However, knowledge on AM symbiosis regulation by CLAVATA signaling is limited. Here, we report a dual role for Medicago truncatula CRN in development and plant–microbe interactions. In shoots, MtCRN modulates inflorescence meristem branching. In roots, the MtCRN promoter is active in vascular tissues and meristematic regions. In addition, MtCRN expression is activated in cortex cells colonized by AM fungi and negatively regulates root interactions with these microbes in a nitrogen-dependent manner; negative AM symbiosis regulation by CRN was also observed in the monocot Zea mays, suggesting this function is conserved across plant clades. We further report that MtCRN functions partially independently of the AM autoregulation signal MtCLE53. Transcriptomic data revealed that M. truncatula crn roots display signs of perturbed nutrient, symbiosis, and stress signaling, suggesting that MtCRN plays various roles in plant development and interactions with the environment.
View Publication(DOI: 10.1093/jxb/eraf386)Medicago truncatula CORYNE regulates inflorescence meristem branching, nutrient signaling, and arbuscular mycorrhizal symbiosis
Authors: Johnathan Orosz, Erica Xinlei Lin, Penelope Lindsay, Mikayla Kappes, Sagar Bashyal, Hasani Everett, Chandan Kumar Gautam, David Jackson, Lena Mueller
Venue: bioRxiv
Published: 2024
The CLAVATA signaling pathway regulates plant development and plant-environment interactions. CLAVATA signaling consists of mobile, cell-type or environment-specific CLAVATA3/ESR-related (CLE) peptides, which are perceived by a receptor complex consisting of leucine-rich repeat receptor-like kinases such as CLAVATA1 and receptor-like proteins such as CLAVATA2, which often functions with the pseudokinase CORYNE (CRN). CLAVATA signaling has been extensively studied in various plant species for its role in meristem maintenance and in legumes for modulating root interactions with nitrogen-fixing rhizobia. Some signaling proteins involved in development and nodulation, including CLAVATA1, also regulate plant interactions with mutualistic arbuscular mycorrhizal (AM) fungi. However, our knowledge on AM symbiosis regulation by CLAVATA signaling remains limited and only a handful of genetic regulators have been identified. Here we report that Medicago truncatula CRN controls inflorescence meristem branching and negatively regulates root interactions with AM fungi. MtCRN functions partially independently of the AM autoregulation signal MtCLE53. Transcriptomic data revealed that crn roots display signs of perturbed signaling related to a range of responses to biotic and abiotic factors, suggesting that MtCRN plays various roles in plant development and interactions with the environment.
Cultivating potential: Harnessing plant stem cells for agricultural crop improvement
Authors: Penelope Lindsay, Kyle W. Swentowsky, David Jackson
Venue: Molecular Plant
Published: 2024
Meristems are stem cell-containing structures that produce all plant organs and are therefore important targets for crop improvement. Developmental regulators control the balance and rate of cell divisions within the meristem. Altering these regulators impacts meristem architecture and, as a consequence, plant form. In this review, we discuss genes involved in regulating the shoot apical meristem, inflorescence meristem, axillary meristem, root apical meristem, and vascular cambium in plants. We highlight several examples showing how crop breeders have manipulated developmental regulators to modify meristem growth and alter crop traits such as inflorescence size and branching patterns. Plant transformation techniques are another innovation related to plant meristem research because they make crop genome engineering possible. We discuss recent advances on plant transformation made possible by studying genes controlling meristem development. Finally, we conclude with discussions about how meristem research can contribute to crop improvement in the coming decades.
View Publication(DOI: 10.1016/j.molp.2023.12.014)Distinct ankyrin repeat subdomains control VAPYRIN locations and intracellular accommodation functions during arbuscular mycorrhizal symbiosis
Authors: Penelope L. Lindsay, Sergey Ivanov, Nathan Pumplin, Xinchun Zhang, Maria J. Harrison
Venue: Nature Communications
Published: 2022
Over 70% of vascular flowering plants engage in endosymbiotic associations with arbuscular mycorrhizal (AM) fungi. VAPYRIN (VPY) is a plant protein that is required for intracellular accommodation of AM fungi but how it functions is still unclear. VPY has a large ankyrin repeat domain with potential for interactions with multiple proteins. Here we show that overexpression of the ankyrin repeat domain results in a vpy-like phenotype, consistent with the sequestration of interacting proteins. We identify distinct ankyrin repeats that are essential for intracellular accommodation of arbuscules and reveal that VPY functions in both the cytoplasm and nucleus. VPY interacts with two kinases, including DOES NOT MAKE INFECTIONS3 (DMI3), a nuclear-localized symbiosis signaling kinase. Overexpression of VPY in a symbiosis-attenuated genetic background results in a dmi3 -like phenotype suggesting that VPY negatively influences DMI3 function. Overall, the data indicate a requirement for VPY in the nucleus and cytoplasm where it may coordinate signaling and cellular accommodation processes.
View Publication(DOI: 10.1038/s41467-022-32124-3)Next Generation Cereal Crop Yield Enhancement: From Knowledge of Inflorescence Development to Practical Engineering by Genome Editing
Authors: Lei Liu, Penelope L. Lindsay, David Jackson
Venue: International Journal of Molecular Sciences
Published: 2021
Artificial domestication and improvement of the majority of crops began approximately 10,000 years ago, in different parts of the world, to achieve high productivity, good quality, and widespread adaptability. It was initiated from a phenotype-based selection by local farmers and developed to current biotechnology-based breeding to feed over 7 billion people. For most cereal crops, yield relates to grain production, which could be enhanced by increasing grain number and weight. Grain number is typically determined during inflorescence development. Many mutants and genes for inflorescence development have already been characterized in cereal crops. Therefore, optimization of such genes could fine-tune yield-related traits, such as grain number. With the rapidly advancing genome-editing technologies and understanding of yield-related traits, knowledge-driven breeding by design is becoming a reality. This review introduces knowledge about inflorescence yield-related traits in cereal crops, focusing on rice, maize, and wheat. Next, emerging genome-editing technologies and recent studies that apply this technology to engineer crop yield improvement by targeting inflorescence development are reviewed. These approaches promise to usher in a new era of breeding practice.
View Publication(DOI: 10.3390/ijms22105167)Rapid expression of COVID-19 proteins by transient expression in tobacco
Authors: Penelope Lindsay, Amanda Ackerman, Yinan Jian, Oliver Artz, Daniele Rosado, Tara Skopelitis, Munenori Kitagawa, Ullas V. Pedmale, David Jackson
Venue: bioRxiv
Published: 2020
In 2020 we suffered from a major global pandemic caused by the SARS-CoV-2 coronavirus. Efforts to contain the virus include the development of rapid tests and vaccines, which require a ready supply of viral proteins. Here we report the production of two SARS-CoV-2 proteins by transient transformation of tobacco, leading to high expression within three days, and subsequent purification of the intact proteins. Such efforts may help to develop testing resources to alleviate the major impacts of this global pandemic.
View Publication(DOI: 10.1101/2020.12.29.424712)A Phosphate-Dependent Requirement for Transcription Factors IPD3 and IPD3L During Arbuscular Mycorrhizal Symbiosis in Medicago truncatula
Authors: Penelope L. Lindsay, Brandon N. Williams, Allyson MacLean, Maria J. Harrison
Venue: Molecular Plant-Microbe Interactions
Published: 2019
During arbuscular mycorrhizal (AM) symbiosis, activation of a symbiosis signaling pathway induces gene expression necessary for accommodation of AM fungi. Here, we focus on pathway components Medicago truncatula INTERACTING PROTEIN OF DOES NOT MAKE INFECTIONS 3 (IPD3) and IPD3 LIKE (IPD3L), which are potential orthologs of Lotus japonicus CYCLOPS, a transcriptional regulator essential for AM symbiosis. In the double mutant ipd3 ipd3l, hyphal entry through the epidermis and overall colonization levels are reduced relative to the wild type but fully developed arbuscules are present in the cortex. In comparison with the wild type, colonization of ipd3 ipd3l is acutely sensitive to higher phosphate levels in the growth medium, with a disproportionate decrease in epidermal penetration, overall colonization, and symbiotic gene expression. When constitutively expressed in ipd3 ipd3l, an autoactive DOES NOT MAKE INFECTIONS 3 induces the expression of transcriptional regulators REDUCED ARBUSCULAR MYCORRHIZA 1 and REQUIRED for ARBUSCULE DEVELOPMENT 1, providing a possible avenue for arbuscule development in the absence of IPD3 and IPD3L. An increased sensitivity of ipd3 ipd3l to GA3 suggests an involvement of DELLA. The data reveal partial redundancy in the symbiosis signaling pathway, which may ensure robust signaling in low-phosphorus environments, while IPD3 and IPD3L maintain signaling in higher-phosphorus environments. The latter may buffer the pathway from short-term variation in phosphorus levels encountered by roots during growth in heterogeneous soil environments.
View Publication(DOI: 10.1094/MPMI-01-19-0006-R)Genetic mapping shows intraspecific variation and transgressive segregation for caterpillar-induced aphid resistance in maize
Authors: Vered Tzin, Penelope L. Lindsay, Shawn A. Christensen, Lisa N. Meihls, Levi B. Blue, Georg Jander
Venue: Molecular Ecology
Published: 2015
Plants in nature have inducible defences that sometimes lead to targeted resistance against particular herbivores, but susceptibility to others. The metabolic diversity and genetic resources available for maize (Zea mays) make this a suitable system for a mechanistic study of within-species variation in such plant-mediated interactions between herbivores. Beet armyworms (Spodoptera exigua) and corn leaf aphids (Rhopalosiphum maidis) are two naturally occurring maize herbivores with different feeding habits. Whereas chewing herbivore-induced methylation of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside (DIMBOA-Glc) to form 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside (HDMBOA-Glc) promotes caterpillar resistance, lower DIMBOA-Glc levels favour aphid reproduction. Thus, caterpillar-induced DIMBOA-Glc methyltransferase activity in maize is predicted to promote aphid growth. To test this hypothesis, the impact of S. exigua feeding on R. maidis progeny production was assessed using seventeen genetically diverse maize inbred lines. Whereas aphid progeny production was increased by prior caterpillar feeding on lines B73, Ki11, Ki3 and Tx303, it decreased on lines Ky21, CML103, Mo18W and W22. Genetic mapping of this trait in a population of B73 × Ky21 recombinant inbred lines identified significant quantitative trait loci on maize chromosomes 1, 7 and 10. There is a transgressive segregation for aphid resistance, with the Ky21 alleles on chromosomes 1 and 7 and the B73 allele on chromosome 10 increasing aphid progeny production. The chromosome 1 QTL coincides with a cluster of three maize genes encoding benzoxazinoid O-methyltransferases that convert DIMBOA-Glc to HDMBOA-Glc. Gene expression studies and benzoxazinoid measurements indicate that S. exigua -induced responses in this pathway differentially affect R. maidis resistance in B73 and Ky21.
View Publication(DOI: 10.1111/mec.13418)