Zhongchi Liu | University of Maryland, College Park (original) (raw)
Papers by Zhongchi Liu
Frontiers in Plant Science
Rosaceae, a large plant family of more than 3,000 species, consists of many economically importan... more Rosaceae, a large plant family of more than 3,000 species, consists of many economically important fruit and ornamental crops, including peach, apple, strawberry, raspberry, cherry, and rose. These horticultural crops are not only important economic drivers in many regions of the world, but also major sources of human nutrition. Additionally, due to the diversity of fruit types in Rosaceae, this plant family offers excellent opportunities for investigations into fleshy fruit diversity, evolution, and development. With the development of high-throughput sequencing technologies and computational tools, an increasing number of high-quality genomes and transcriptomes of Rosaceae species have become available and will greatly facilitate Rosaceae research and breeding. This review summarizes major genomic resources and genome research progress in Rosaceae, highlights important databases, and suggests areas for further improvement. The availability of these big data resources will greatly ...
Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Beca... more Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Because of their photosynthetic efficiency and high-lipid content, diatoms are priority candidates for biofuel production. Here, we report that sporulating Bacillus thuringiensis when in co-culture with a marine diatom Phaeodactylum tricornutum significantly increases the diatom cell count. Bioassay-guided purification led to the identification of two diketopiperazines (DKPs) that both stimulate P. tricornutum growth and increase its lipid content. RNA-seq analysis revealed upregulation of a small set of P. tricornutum genes involved in iron starvation response and nutrient recycling when DKP was added to the diatom culture. This work demonstrates that two DKPs produced by a bacterium could positively impact P. tricornutum growth and lipid content, offering new approaches to enhance P. tricornutum-based biofuel production. As increasing numbers of DKPs are isolated from marine microbes, the ...
Development, 2019
In the Arabidopsis stomatal lineage, cells transit through several distinct precursor identities,... more In the Arabidopsis stomatal lineage, cells transit through several distinct precursor identities, each characterized by unique cell division behaviors. Flexibility in the duration of these precursor phases enables plants to alter leaf size and stomatal density in response to environmental conditions; however, transitions between phases must be complete and unidirectional to produce functional and correctly patterned stomata. Among direct transcriptional targets of the stomatal initiating factor, SPEECHLESS, a pair of genes, SOL1 and SOL2, are required for effective transitions in the lineage. We show that these two genes, which are homologues of the LIN54 DNA-binding components of the mammalian DREAM complex, are expressed in a cell cycle dependent manner and regulate cell fate and division properties in the self-renewing early lineage. In the terminal division of the stomatal lineage, however, these two proteins appear to act in opposition to their closest paralogue, TSO1, revealin...
PLoS pathogens, Jun 15, 2018
Iron is essential for many cellular processes, but can generate highly toxic hydroxyl radicals in... more Iron is essential for many cellular processes, but can generate highly toxic hydroxyl radicals in the presence of oxygen. Therefore, intracellular iron accumulation must be tightly regulated, by balancing uptake with storage or export. Iron uptake in Leishmania is mediated by the coordinated action of two plasma membrane proteins, the ferric iron reductase LFR1 and the ferrous iron transporter LIT1. However, how these parasites regulate their cytosolic iron concentration to prevent toxicity remains unknown. Here we characterize Leishmania Iron Regulator 1 (LIR1), an iron responsive protein with similarity to membrane transporters of the major facilitator superfamily (MFS) and plant nodulin-like proteins. LIR1 localizes on the plasma membrane of L. amazonensis promastigotes and intracellular amastigotes. After heterologous expression in Arabidopsis thaliana, LIR1 decreases the iron content of leaves and worsens the chlorotic phenotype of plants lacking the iron importer IRT1. Consist...
Molecular plant, Jan 17, 2017
Proceedings of the National Academy of Sciences, 2004
Transcription repression plays important roles in preventing crucial regulatory proteins from bei... more Transcription repression plays important roles in preventing crucial regulatory proteins from being expressed in inappropriate temporal or spatial domains. LEUNIG ( LUG ) and SEUSS ( SEU ) normally act to prevent ectopic expression of the floral homeotic gene AGAMOUS in flowers. LUG encodes a protein with sequence similarities to the yeast Tup1 corepressor. SEU encodes a plant-specific regulatory protein with sequence similarity in a conserved dimerization domain to the LIM-domain binding 1/Chip proteins in mouse and Drosophila . Despite the molecular isolation of LUG and SEU , the biochemical function of these two proteins remains uncharacterized, and the mechanism of AGAMOUS repression remains unknown. Here, we report that LUG and SEU interact directly in vitro and in vivo . Furthermore, LUG exhibits a strong repressor activity on several heterologous promoters in yeast and plant cells. SEU, in contrast, does not exhibit any direct repressor activity, but can repress reporter gene...
Development, 2006
The transcriptional repression of key regulatory genes is crucial for plant and animal developmen... more The transcriptional repression of key regulatory genes is crucial for plant and animal development. Previously, we identified and isolated two Arabidopsis transcription co-repressors LEUNIG(LUG) and SEUSS (SEU) that function together in a putative co-repressor complex to prevent ectopic AGAMOUS(AG) transcription in flowers. Because neither LUG nor SEU possesses a recognizable DNA-binding motif, how they are tethered to specific target promoters remains unknown. Using the yeast two-hybrid assay and a co-immunoprecipitation assay, we showed that APETALA1 (AP1)and SEPALLATA3 (SEP3), both MADS box DNA-binding proteins,interacted with SEU. The AP1-SEU protein-protein interaction was supported by synergistic genetic interactions between ap1 and seu mutations. The role of SEU proteins in bridging the interaction between AP1/SEP3 and LUG to repress target gene transcription was further demonstrated in yeast and plant cells, providing important mechanistic insights into co-repressor function...
Nature Communications
The dominance of flowering plants on earth is owed largely to the evolution of maternal tissues s... more The dominance of flowering plants on earth is owed largely to the evolution of maternal tissues such as fruit and seedcoat that protect and disseminate the seeds. The mechanism of how fertilization triggers the development of these specialized maternal tissues is not well understood. A key event is the induction of auxin synthesis in the endosperm, and the mobile auxin subsequently stimulates seedcoat and fruit development. However, the regulatory mechanism of auxin synthesis in the endosperm remains unknown. Here, we show that a type I MADS box gene AGL62 is required for the activation of auxin synthesis in the endosperm in both Fragaria vesca, a diploid strawberry, and in Arabidopsis. Several strawberry FveATHB genes were identified as downstream targets of FveAGL62 and act to repress auxin biosynthesis. In this work, we identify a key mechanism for auxin induction to mediate fertilization success, a finding broadly relevant to flowering plants.
Horticulture research, 2017
Wild strawberry Fragaria vesca is emerging as an important model system for the cultivated strawb... more Wild strawberry Fragaria vesca is emerging as an important model system for the cultivated strawberry due to its diploid genome and availability of extensive transcriptome data and a range of molecular genetic tools. Being able to better utilize these tools, especially the transcriptome data, will greatly facilitate research progress in strawberry and other Rosaceae fruit crops. The electronic fluorescent pictograph (eFP) software is a useful and popular tool to display transcriptome data visually, and is widely used in other model organisms including Arabidopsis and mouse. Here we applied eFP to display wild strawberry RNA sequencing (RNA-seq) data from 42 different tissues and stages, including various flower and fruit developmental stages. In addition, we generated eight additional RNA-seq data sets to represent tissues from ripening-stage receptacle fruit from yellow-colored and red-colored wild strawberry varieties. Differential gene expression analysis between these eight data...
Proceedings of the National Academy of Sciences, 2018
Significance Plant postembryonic development relies on a small pool of stem cells at the shoot an... more Significance Plant postembryonic development relies on a small pool of stem cells at the shoot and root tip. The question of how the cell cycle regulatory activities are integrated into the specific stem cell context is not well understood. This study identifies a previously unknown regulatory module in the flowering plant consisting of two regulatory genes, TSO1 and MYB3R1 . TSO1 negatively regulates MYB3R1 to control cell division activity, maintain proper stem cell pool size, and balance cell proliferation with differentiation in shoot and root. Significantly, animal homologs of TSO1 and MYB3R1 are members of a cell cycle regulatory complex, suggesting that this conserved module operates in both plants and animals.
Plant Physiology
Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Beca... more Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Because of their photosynthetic efficiency and high-lipid content, diatoms are priority candidates for biofuel production. Here, we report that sporulating Bacillus thuringiensis and other members of the Bacillus cereus group, when in co-culture with the marine diatom Phaeodactylum tricornutum, significantly increase diatom cell count. Bioassay-guided purification of the mother cell lysate of B. thuringiensis led to the identification of two diketopiperazines (DKPs) that stimulate both P. tricornutum growth and increase its lipid content. These findings may be exploited to enhance P. tricornutum growth and microalgae-based biofuel production. As increasing numbers of DKPs are isolated from marine microbes, the work gives potential clues to bacterial-produced growth factors for marine microalgae.
Plant Physiology
Unlike ovary-derived botanical fruits, strawberry (Fragaria x ananassa) is an accessory fruit der... more Unlike ovary-derived botanical fruits, strawberry (Fragaria x ananassa) is an accessory fruit derived from the receptacle, the stem tip subtending floral organs. Although both botanical and accessory fruits initiate development in response to auxin and gibberellic acid (GA) released from seeds, the downstream auxin and GA signaling mechanisms underlying accessory fruit development are presently unknown. We characterized GA and auxin signaling mutants in wild strawberry (Fragaria vesca) during early stage fruit development. While mutations in FveRGA1 and FveARF8 both led to the development of larger fruit, only mutations in FveRGA1 caused parthenocarpic fruit formation, suggesting FveRGA1 is a key regulator of fruit set. FveRGA1 mediated fertilization-induced GA signaling during accessory fruit initiation by repressing the expression of cell division and expansion genes and showed direct protein–protein interaction with FveARF8. Further, fvearf8 mutant fruits exhibited an enhanced re...
Current Opinion in Plant Biology
Annual Review of Plant Biology
Rosaceae (the rose family) is an economically important family that includes species prized for h... more Rosaceae (the rose family) is an economically important family that includes species prized for high-value fruits and ornamentals. The family also exhibits diverse fruit types, including drupe (peach), pome (apple), drupetum (raspberry), and achenetum (strawberry). Phylogenetic analysis and ancestral fruit-type reconstruction suggest independent evolutionary paths of multiple fleshy fruit types from dry fruits. A recent whole genome duplication in the Maleae/Pyreae tribe (with apple, pear, hawthorn, and close relatives; referred to as Maleae here) may have contributed to the evolution of pome fruit. MADS-box genes, known to regulate floral organ identity, are emerging as important regulators of fruit development. The differential competence of floral organs to respond to fertilization signals may explain the different abilities of floral organs to form fleshy fruit. Future comparative genomics and functional studies in closely related Rosaceae species with distinct fruit types will ...
Strawberry, a high value fruit crop, has recently become amenable for genetic studies due to geno... more Strawberry, a high value fruit crop, has recently become amenable for genetic studies due to genomic resources and CRISPR/CAS9 tools. Unlike ovary-derived botanical fruits, strawberry is an accessory fruit derived from receptacle, the stem tip subtending floral organs. Although both botanical and accessory fruits initiate development in response to auxin and GA released from seeds, the downstream auxin and GA signaling mechanisms underlying accessory fruit development remain unknown. Using wild strawberry, we performed in depth molecular characterizations of accessory fruit development. We show that auxin signaling proteins FveARF8/FveARF6 are bound and hence inhibited by FveIAA4 and FveRGA1, repressors in auxin and GA signaling pathways. This inhibition is relieved post-fertilization or by the application of GA or auxin. Mutants of FveRGA1 developed parthenocarpic fruit suggesting a conserved function of DELLA proteins in fruit set. Further, FveARF8 was found to repress the express...
Frontiers in Plant Science
Rosaceae, a large plant family of more than 3,000 species, consists of many economically importan... more Rosaceae, a large plant family of more than 3,000 species, consists of many economically important fruit and ornamental crops, including peach, apple, strawberry, raspberry, cherry, and rose. These horticultural crops are not only important economic drivers in many regions of the world, but also major sources of human nutrition. Additionally, due to the diversity of fruit types in Rosaceae, this plant family offers excellent opportunities for investigations into fleshy fruit diversity, evolution, and development. With the development of high-throughput sequencing technologies and computational tools, an increasing number of high-quality genomes and transcriptomes of Rosaceae species have become available and will greatly facilitate Rosaceae research and breeding. This review summarizes major genomic resources and genome research progress in Rosaceae, highlights important databases, and suggests areas for further improvement. The availability of these big data resources will greatly ...
Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Beca... more Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Because of their photosynthetic efficiency and high-lipid content, diatoms are priority candidates for biofuel production. Here, we report that sporulating Bacillus thuringiensis when in co-culture with a marine diatom Phaeodactylum tricornutum significantly increases the diatom cell count. Bioassay-guided purification led to the identification of two diketopiperazines (DKPs) that both stimulate P. tricornutum growth and increase its lipid content. RNA-seq analysis revealed upregulation of a small set of P. tricornutum genes involved in iron starvation response and nutrient recycling when DKP was added to the diatom culture. This work demonstrates that two DKPs produced by a bacterium could positively impact P. tricornutum growth and lipid content, offering new approaches to enhance P. tricornutum-based biofuel production. As increasing numbers of DKPs are isolated from marine microbes, the ...
Development, 2019
In the Arabidopsis stomatal lineage, cells transit through several distinct precursor identities,... more In the Arabidopsis stomatal lineage, cells transit through several distinct precursor identities, each characterized by unique cell division behaviors. Flexibility in the duration of these precursor phases enables plants to alter leaf size and stomatal density in response to environmental conditions; however, transitions between phases must be complete and unidirectional to produce functional and correctly patterned stomata. Among direct transcriptional targets of the stomatal initiating factor, SPEECHLESS, a pair of genes, SOL1 and SOL2, are required for effective transitions in the lineage. We show that these two genes, which are homologues of the LIN54 DNA-binding components of the mammalian DREAM complex, are expressed in a cell cycle dependent manner and regulate cell fate and division properties in the self-renewing early lineage. In the terminal division of the stomatal lineage, however, these two proteins appear to act in opposition to their closest paralogue, TSO1, revealin...
PLoS pathogens, Jun 15, 2018
Iron is essential for many cellular processes, but can generate highly toxic hydroxyl radicals in... more Iron is essential for many cellular processes, but can generate highly toxic hydroxyl radicals in the presence of oxygen. Therefore, intracellular iron accumulation must be tightly regulated, by balancing uptake with storage or export. Iron uptake in Leishmania is mediated by the coordinated action of two plasma membrane proteins, the ferric iron reductase LFR1 and the ferrous iron transporter LIT1. However, how these parasites regulate their cytosolic iron concentration to prevent toxicity remains unknown. Here we characterize Leishmania Iron Regulator 1 (LIR1), an iron responsive protein with similarity to membrane transporters of the major facilitator superfamily (MFS) and plant nodulin-like proteins. LIR1 localizes on the plasma membrane of L. amazonensis promastigotes and intracellular amastigotes. After heterologous expression in Arabidopsis thaliana, LIR1 decreases the iron content of leaves and worsens the chlorotic phenotype of plants lacking the iron importer IRT1. Consist...
Molecular plant, Jan 17, 2017
Proceedings of the National Academy of Sciences, 2004
Transcription repression plays important roles in preventing crucial regulatory proteins from bei... more Transcription repression plays important roles in preventing crucial regulatory proteins from being expressed in inappropriate temporal or spatial domains. LEUNIG ( LUG ) and SEUSS ( SEU ) normally act to prevent ectopic expression of the floral homeotic gene AGAMOUS in flowers. LUG encodes a protein with sequence similarities to the yeast Tup1 corepressor. SEU encodes a plant-specific regulatory protein with sequence similarity in a conserved dimerization domain to the LIM-domain binding 1/Chip proteins in mouse and Drosophila . Despite the molecular isolation of LUG and SEU , the biochemical function of these two proteins remains uncharacterized, and the mechanism of AGAMOUS repression remains unknown. Here, we report that LUG and SEU interact directly in vitro and in vivo . Furthermore, LUG exhibits a strong repressor activity on several heterologous promoters in yeast and plant cells. SEU, in contrast, does not exhibit any direct repressor activity, but can repress reporter gene...
Development, 2006
The transcriptional repression of key regulatory genes is crucial for plant and animal developmen... more The transcriptional repression of key regulatory genes is crucial for plant and animal development. Previously, we identified and isolated two Arabidopsis transcription co-repressors LEUNIG(LUG) and SEUSS (SEU) that function together in a putative co-repressor complex to prevent ectopic AGAMOUS(AG) transcription in flowers. Because neither LUG nor SEU possesses a recognizable DNA-binding motif, how they are tethered to specific target promoters remains unknown. Using the yeast two-hybrid assay and a co-immunoprecipitation assay, we showed that APETALA1 (AP1)and SEPALLATA3 (SEP3), both MADS box DNA-binding proteins,interacted with SEU. The AP1-SEU protein-protein interaction was supported by synergistic genetic interactions between ap1 and seu mutations. The role of SEU proteins in bridging the interaction between AP1/SEP3 and LUG to repress target gene transcription was further demonstrated in yeast and plant cells, providing important mechanistic insights into co-repressor function...
Nature Communications
The dominance of flowering plants on earth is owed largely to the evolution of maternal tissues s... more The dominance of flowering plants on earth is owed largely to the evolution of maternal tissues such as fruit and seedcoat that protect and disseminate the seeds. The mechanism of how fertilization triggers the development of these specialized maternal tissues is not well understood. A key event is the induction of auxin synthesis in the endosperm, and the mobile auxin subsequently stimulates seedcoat and fruit development. However, the regulatory mechanism of auxin synthesis in the endosperm remains unknown. Here, we show that a type I MADS box gene AGL62 is required for the activation of auxin synthesis in the endosperm in both Fragaria vesca, a diploid strawberry, and in Arabidopsis. Several strawberry FveATHB genes were identified as downstream targets of FveAGL62 and act to repress auxin biosynthesis. In this work, we identify a key mechanism for auxin induction to mediate fertilization success, a finding broadly relevant to flowering plants.
Horticulture research, 2017
Wild strawberry Fragaria vesca is emerging as an important model system for the cultivated strawb... more Wild strawberry Fragaria vesca is emerging as an important model system for the cultivated strawberry due to its diploid genome and availability of extensive transcriptome data and a range of molecular genetic tools. Being able to better utilize these tools, especially the transcriptome data, will greatly facilitate research progress in strawberry and other Rosaceae fruit crops. The electronic fluorescent pictograph (eFP) software is a useful and popular tool to display transcriptome data visually, and is widely used in other model organisms including Arabidopsis and mouse. Here we applied eFP to display wild strawberry RNA sequencing (RNA-seq) data from 42 different tissues and stages, including various flower and fruit developmental stages. In addition, we generated eight additional RNA-seq data sets to represent tissues from ripening-stage receptacle fruit from yellow-colored and red-colored wild strawberry varieties. Differential gene expression analysis between these eight data...
Proceedings of the National Academy of Sciences, 2018
Significance Plant postembryonic development relies on a small pool of stem cells at the shoot an... more Significance Plant postembryonic development relies on a small pool of stem cells at the shoot and root tip. The question of how the cell cycle regulatory activities are integrated into the specific stem cell context is not well understood. This study identifies a previously unknown regulatory module in the flowering plant consisting of two regulatory genes, TSO1 and MYB3R1 . TSO1 negatively regulates MYB3R1 to control cell division activity, maintain proper stem cell pool size, and balance cell proliferation with differentiation in shoot and root. Significantly, animal homologs of TSO1 and MYB3R1 are members of a cell cycle regulatory complex, suggesting that this conserved module operates in both plants and animals.
Plant Physiology
Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Beca... more Diatoms are photosynthetic microalgae that fix a significant fraction of the world’s carbon. Because of their photosynthetic efficiency and high-lipid content, diatoms are priority candidates for biofuel production. Here, we report that sporulating Bacillus thuringiensis and other members of the Bacillus cereus group, when in co-culture with the marine diatom Phaeodactylum tricornutum, significantly increase diatom cell count. Bioassay-guided purification of the mother cell lysate of B. thuringiensis led to the identification of two diketopiperazines (DKPs) that stimulate both P. tricornutum growth and increase its lipid content. These findings may be exploited to enhance P. tricornutum growth and microalgae-based biofuel production. As increasing numbers of DKPs are isolated from marine microbes, the work gives potential clues to bacterial-produced growth factors for marine microalgae.
Plant Physiology
Unlike ovary-derived botanical fruits, strawberry (Fragaria x ananassa) is an accessory fruit der... more Unlike ovary-derived botanical fruits, strawberry (Fragaria x ananassa) is an accessory fruit derived from the receptacle, the stem tip subtending floral organs. Although both botanical and accessory fruits initiate development in response to auxin and gibberellic acid (GA) released from seeds, the downstream auxin and GA signaling mechanisms underlying accessory fruit development are presently unknown. We characterized GA and auxin signaling mutants in wild strawberry (Fragaria vesca) during early stage fruit development. While mutations in FveRGA1 and FveARF8 both led to the development of larger fruit, only mutations in FveRGA1 caused parthenocarpic fruit formation, suggesting FveRGA1 is a key regulator of fruit set. FveRGA1 mediated fertilization-induced GA signaling during accessory fruit initiation by repressing the expression of cell division and expansion genes and showed direct protein–protein interaction with FveARF8. Further, fvearf8 mutant fruits exhibited an enhanced re...
Current Opinion in Plant Biology
Annual Review of Plant Biology
Rosaceae (the rose family) is an economically important family that includes species prized for h... more Rosaceae (the rose family) is an economically important family that includes species prized for high-value fruits and ornamentals. The family also exhibits diverse fruit types, including drupe (peach), pome (apple), drupetum (raspberry), and achenetum (strawberry). Phylogenetic analysis and ancestral fruit-type reconstruction suggest independent evolutionary paths of multiple fleshy fruit types from dry fruits. A recent whole genome duplication in the Maleae/Pyreae tribe (with apple, pear, hawthorn, and close relatives; referred to as Maleae here) may have contributed to the evolution of pome fruit. MADS-box genes, known to regulate floral organ identity, are emerging as important regulators of fruit development. The differential competence of floral organs to respond to fertilization signals may explain the different abilities of floral organs to form fleshy fruit. Future comparative genomics and functional studies in closely related Rosaceae species with distinct fruit types will ...
Strawberry, a high value fruit crop, has recently become amenable for genetic studies due to geno... more Strawberry, a high value fruit crop, has recently become amenable for genetic studies due to genomic resources and CRISPR/CAS9 tools. Unlike ovary-derived botanical fruits, strawberry is an accessory fruit derived from receptacle, the stem tip subtending floral organs. Although both botanical and accessory fruits initiate development in response to auxin and GA released from seeds, the downstream auxin and GA signaling mechanisms underlying accessory fruit development remain unknown. Using wild strawberry, we performed in depth molecular characterizations of accessory fruit development. We show that auxin signaling proteins FveARF8/FveARF6 are bound and hence inhibited by FveIAA4 and FveRGA1, repressors in auxin and GA signaling pathways. This inhibition is relieved post-fertilization or by the application of GA or auxin. Mutants of FveRGA1 developed parthenocarpic fruit suggesting a conserved function of DELLA proteins in fruit set. Further, FveARF8 was found to repress the express...