About

Robert Franks is a professor in the Department of Plant and Microbial Biology at North Carolina State University, with research focused on plant developmental biology, particularly the mechanisms regulating organ size, shape, and patterning within the carpel of flowering plants. His work emphasizes understanding the transcriptional gene regulatory networks controlling ovule initiation and meristematic competence in the carpel margin meristems (CMMs), which are analogous to mammalian ovaries and placentas. His research also investigates the identification and functional analysis of novel genes involved in CMM development, utilizing techniques such as fluorescent activated cell sorting (FACS) to isolate specific cell populations. Additionally, Dr. Franks collaborates on studies related to hybrid seed inviability and the evolution of endosperm development in Mimulus species, exploring molecular mechanisms of reproductive isolation and speciation. His contributions extend to understanding the genetic and developmental basis of seed development, with implications for agriculture and evolutionary biology.

Research topics

• Genetics
• Botany
• Cell biology
• Biology
• Computational biology

Selected publications

• Machine Learning Inference of Gene Regulatory Networks in Developing Mimulus Seeds

  Plants · 2024-11-23 · 2 citations

  articleOpen accessSenior authorCorresponding

  The angiosperm seed represents a critical evolutionary breakthrough that has been shown to propel the reproductive success and radiation of flowering plants. Seeds promote the rapid diversification of angiosperms by establishing postzygotic reproductive barriers, such as hybrid seed inviability. While prezygotic barriers to reproduction tend to be transient, postzygotic barriers are often permanent and therefore can play a pivotal role in facilitating speciation. This property of the angiosperm seed is exemplified in the Mimulus genus. In order to further the understanding of the gene regulatory mechanisms important in the Mimulus seed, we performed gene regulatory network (GRN) inference analysis by using time-series RNA-seq data from developing hybrid seeds from a viable cross between Mimulus guttatus and Mimulus pardalis. GRN inference has the capacity to identify active regulatory mechanisms in a sample and highlight genes of potential biological importance. In our case, GRN inference also provided the opportunity to uncover active regulatory relationships and generate a reference set of putative gene regulations. We deployed two GRN inference algorithms—RTP-STAR and KBoost—on three different subsets of our transcriptomic dataset. While the two algorithms yielded GRNs with different regulations and topologies when working with the same data subset, there was still significant overlap in the specific gene regulations they inferred, and they both identified potential novel regulatory mechanisms that warrant further investigation.

  PublisherDOI

• Assessing the role of REM13, REM34 and REM46 during the transition to the reproductive phase in Arabidopsis thaliana

  Plant Molecular Biology · 2023 · 9 citations

  • Biology
  • Genetics
  • Cell biology

  REM (reproductive meristem) transcription factors have been proposed as regulators of plant reproductive development mainly based on their specific expression patterns in reproductive structures, but their roles are still largely unknown probably because of their redundancy. We selected three REM genes (REM13, REM34 and REM46) for functional analysis, based on their genome position and/or co-expression data.Our results suggest that these genes have a role in flowering time regulation and may modulate cell cycle progression. In addition, protein interaction experiments revealed that REM34 and REM46 interact with each other, suggesting that they might work cooperatively to regulate cell division during inflorescence meristem commitment.Previous attempts of using co-expression data as a guide for functional analysis of REMs were limited by the transcriptomic data available at the time. Our results uncover previously unknown functions of three members of the REM family of Arabidopsis thaliana and open the door to more comprehensive studies of the REM family, where the combination of co-expression analysis followed by functional studies might contribute to uncovering the biological roles of these proteins and the relationship among them.

  PublisherOA PDFDOI

• HISTONE DEACETYLASE19 Controls Ovule Number Determination and Transmitting Tract Differentiation

  PLANT PHYSIOLOGY · 2023 · 10 citations

  • Biology
  • Cell biology
  • Genetics

  The gynoecium is critical for the reproduction of flowering plants as it contains the ovules and the tissues that foster pollen germination, growth, and guidance. These tissues, known as the reproductive tract (ReT), comprise the stigma, style, and transmitting tract (TT). The ReT and ovules originate from the carpel margin meristem (CMM) within the pistil. SHOOT MERISTEMLESS (STM) is a key transcription factor for meristem formation and maintenance. In all above-ground meristems, including the CMM, local STM downregulation is required for organ formation. However, how this downregulation is achieved in the CMM is unknown. Here, we have studied the role of HISTONE DEACETYLASE 19 (HDA19) in Arabidopsis (Arabidopsis thaliana) during ovule and ReT differentiation based on the observation that the hda19-3 mutant displays a reduced ovule number and fails to differentiate the TT properly. Fluorescence-activated cell sorting coupled with RNA-sequencing revealed that in the CMM of hda19-3 mutants, genes promoting organ development are downregulated while meristematic markers, including STM, are upregulated. HDA19 was essential to downregulate STM in the CMM, thereby allowing ovule formation and TT differentiation. STM is ectopically expressed in hda19-3 at intermediate stages of pistil development, and its downregulation by RNA interference alleviated the hda19-3 phenotype. Chromatin immunoprecipitation assays indicated that STM is a direct target of HDA19 during pistil development and that the transcription factor SEEDSTICK is also required to regulate STM via histone acetylation. Thus, we identified factors required for the downregulation of STM in the CMM, which is necessary for organogenesis and tissue differentiation.

  PublisherOA PDFDOI

• Developmental Analysis of Mimulus Seed Transcriptomes Reveals Functional Gene Expression Clusters and Four Imprinted, Endosperm-Expressed Genes

  Frontiers in Plant Science · 2020 · 20 citations

  Senior authorCorresponding
  • Biology
  • Genetics
  • Cell biology

  , and will inform future studies on the genetic causes of seed failure in this model system.

  PublisherDOI

• Functional characterization of Terminal Flower1 homolog in Cornus canadensis by genetic transformation

  Plant Cell Reports · 2019-01-07 · 13 citations

  article
  PublisherDOI

• Redundant CArG Box Cis-motif Activity Mediates SHATTERPROOF2 Transcriptional Regulation during Arabidopsis thaliana Gynoecium Development

  Frontiers in Plant Science · 2017-10-16 · 16 citations

  articleOpen accessSenior authorCorresponding

  repression in the valve.

  PublisherDOI

• Alterations of <i>Cor<scp>TFL</scp>1</i> and <i>Cor<scp>AP</scp>1</i> expression correlate with major evolutionary shifts of inflorescence architecture in <i>Cornus</i> (Cornaceae) – a proposed model for variation of closed inflorescence forms

  New Phytologist · 2016-09-23 · 24 citations

  articleOpen accessCorresponding

  TFL1-, AP1- and LFY-like genes are known to be key regulators of inflorescence development. However, it remains to be tested whether the evolutionary modifications of inflorescence morphology result from shifts in their expression patterns. We compared the spatiotemporal expression patterns of CorTFL1, CorAP1 and CorLFY in six closely related Cornus species that display four types of closed inflorescence morphology using quantitative real-time polymerase chain reaction (qRT-PCR) and RNA in situ hybridization. Character mapping on the phylogeny was conducted to identify evolutionary changes and to assess the correlation between changes in gene expression and inflorescence morphology. Results demonstrated variation of gene expression patterns among species and a strong correlation between CorTFL1 expression and the branch index of the inflorescence type. Evolutionary changes in CorTFL1 and CorAP1 expression co-occurred on the phylogeny with the morphological changes underpinning inflorescence divergence. The study found a clear correlation between the expression patterns of CorTFL1 and CorAP1 and the inflorescence architecture in a natural system displaying closed inflorescences. The results suggest a role for the alteration in CorTFL1 and CorAP1 expression during the evolutionary modification of inflorescences in Cornus. We propose that a TFL1-like and AP1-like gene-based model may explain variation of closed inflorescences in Cornus and other lineages.

  PublisherOA PDFDOI

• Analysis of two TFL1 homologs of dogwood species (Cornus L.) indicates functional conservation in control of transition to flowering

  Planta · 2016-01-29 · 58 citations

  article
  PublisherDOI

• Disruption of endosperm development is a major cause of hybrid seed inviability between <i>Mimulus guttatus</i> and <i>Mimulus nudatus</i>

  New Phytologist · 2016-01-29 · 84 citations

  articleOpen accessSenior author

  Divergence of developmental mechanisms within populations could lead to hybrid developmental failure, and might be a factor driving speciation in angiosperms. We investigate patterns of endosperm and embryo development in Mimulus guttatus and the closely related, serpentine endemic Mimulus nudatus, and compare them to those of reciprocal hybrid seed. We address whether disruption in hybrid seed development is the primary source of reproductive isolation between these sympatric taxa. M. guttatus and M. nudatus differ in the pattern and timing of endosperm and embryo development. Some hybrid seeds exhibit early disruption of endosperm development and are completely inviable, while others develop relatively normally at first, but later exhibit impaired endosperm proliferation and low germination success. These developmental patterns are reflected in mature hybrid seeds, which are either small and flat (indicating little to no endosperm) or shriveled (indicating reduced endosperm volume). Hybrid seed inviability forms a potent reproductive barrier between M. guttatus and M. nudatus. We shed light on the extent of developmental variation between closely related species within the M. guttatus species complex, an important ecological model system, and provide a partial mechanism for the hybrid barrier between M. guttatus and M. nudatus.

  PublisherOA PDFDOI

• SEUSS Integrates Gibberellin Signaling with Transcriptional Inputs from the SHR-SCR-SCL3 Module to Regulate Middle Cortex Formation in the Arabidopsis Root

  PLANT PHYSIOLOGY · 2016-01-27 · 63 citations

  articleOpen access

  A decade of studies on middle cortex (MC) formation in the root endodermis of Arabidopsis (Arabidopsis thaliana) have revealed a complex regulatory network that is orchestrated by several GRAS family transcription factors, including SHORT-ROOT (SHR), SCARECROW (SCR), and SCARECROW-LIKE3 (SCL3). However, how their functions are regulated remains obscure. Here we show that mutations in the SEUSS (SEU) gene led to a higher frequency of MC formation. seu mutants had strongly reduced expression of SHR, SCR, and SCL3, suggesting that SEU positively regulates these genes. Our results further indicate that SEU physically associates with upstream regulatory sequences of SHR, SCR, and SCL3; and that SEU has distinct genetic interactions with these genes in the control of MC formation, with SCL3 being epistatic to SEU. Similar to SCL3, SEU was repressed by the phytohormone GA and induced by the GA biosynthesis inhibitor paclobutrazol, suggesting that SEU acts downstream of GA signaling to regulate MC formation. Consistently, we found that SEU mediates the regulation of SCL3 by GA signaling. Together, our study identifies SEU as a new critical player that integrates GA signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate MC formation in the Arabidopsis root.

  PublisherDOI

Recent grants

• NIH Grant F32GM020426

  NIH · $144k

• Collaborative Research: RoL: Rapid Evolution of Reproductive Isolation via Hybrid Seed Lethality in Mimulus

  NSF · $633k · 2019–2025

• Collaborative Research: Hybrid Seed Inviability and the Evolution of Endosperm Development in Mimulus

  NSF · $320k · 2016–2021

• Transcriptional Regulators Link Patterning and Proliferation during Carpel Margin and Ovule Development

  NSF · $424k · 2008–2014

• Transcriptional Nodes Coordinate Patterning and Cellular Proliferation during Carpel Margin Meristem Development

  NSF · $820k · 2014–2019

Frequent coauthors

• Qiu‐Yun Xiang

  North Carolina State University

  8 shared

• Zhongchi Liu

  University of Maryland, College Park

  8 shared

• April N. Wynn

  University of Mary Washington

  5 shared

• Miguel A. Flores‐Vergara

  North Carolina State University

  5 shared

• John H. Willis

  Duke University

  5 shared

• Elen Oneal

  Duke University

  5 shared

• Silvia Manrique

  Universitat Politècnica de València

  4 shared

• Gonzalo Villarino

  Salk Institute for Biological Studies

  4 shared

Labs

• Robert Franks LabPI

Education

• Ph.D., Plant Pathology

  University of California, Berkeley

  1990

• M.S., Plant Pathology

  University of California, Berkeley

  1985

• B.S., Botany

  University of California, Davis

  1983

Awards & honors

• Collaborative Research: RoL: Rapid Evolution of Reproductive…
• Collaborative Research: Hybrid Seed Inviability and the Evol…