Zheng Lab: Nutrient Sensing and Cell Morphogenesis Signaling Networks

 

 

Breakthrough in nutrient sensing:

A sulfate transceptor identified!

SULTR1;2 final.pub.white.png

 

 

 

 

 

 

 

 
PI: Zhi-Liang Zheng (PhD, 1999, Ohio State University)

 

Professor

Department of Biological Sciences

Lehman College

City University of New York

250 Bedford Park Blvd. West

Bronx, NY 10468

 

Office: 2404 Science Hall

Lab: 2401 Science Hall

(718) 960-6955 (Office)

(718) 960-5741 (Lab)

(718) 960-8236 (Fax)

E-mail: zhiliang.zheng@lehman.cuny.edu

 

Teaching

 

BIO 238 Genetics (undergraduate level, 4 credits: 2-hr lecture, 4-hr lab)

BIO 501 Special Topics in Genetics (graduate level, 4 credits: 4-hr lecture)

 

Research

 

Eukaryotes need to respond to dynamic internal cues and external stimuli in order to quickly adapt to their surrounding environments (such as light, temperature, water, CO2 and nutrients). Our research is currently focused on the major nutrients, such as carbon (C), nitrogen (N) and sulfur (S), with a goal of constructing nutrient perception and signal transduction networks and understanding how the nutrient status impacts cell growth and morphogenesis.

 

Novel transcriptional regulatory mechanism in cell morphogenesis  Rho family small GTPases, including Rho, Rac and Cdc42 subfamilies in yeast and animals and ROP subfamily in plants, are best known as key signaling switches in cell growth and shape control. Constitutive activation of Arabidopsis ROP2 in transgenic line CA1-1 has been shown to disrupt cell polarity in both leaf pavement cells and root hairs. Our prior forward genetic studies first showed that the CA1-1 enhancer 1 (cae1-1) mutation, which is allelic to MRH2 kinesin gene, converted all root hairs to the bulbous shape in the CA1-1 background (Yang et al., 2007). This finding indicates that MRH2 might be involved in interacting with ROP2 signaling to control the microtubule organization and coordinate with actin filaments.

 

We recently characterized the cae2-1 enhancer mutant, leading us to discover the first transcriptional regulatory mechanism for plant pavement cell shape determination (Zhang et al., 2016). Specifically, we found that cae2-1 is allelic to cpl1 or fry2, indicating that the RNA polymerase II (Pol II) C-terminal domain (CTD) phosphatase CPL1 is a critical transcriptional regulator in ROP2-mediated gene expression. Posttranscriptional modifications in the CTD heptad peptide repeats (Y1S2P3T4S5P6S7), in particular phosphorylation at Ser2 and Ser5, are collectively called the “CTD code” and critical for completing transcriptional cycles for almost all protein-coding genes. Our genetic and biochemical evidence has shown that ROP2 stimulates CTD Ser2 and Ser5 phosphorylation by inhibiting CPL1 phosphatase. Furthermore, we showed a similar CTD phosphatase degradation mechanism in yeast Rho GTPase control of cell shape. These results provide convincing evidence that Rho GTPase and Pol II, two key molecules which have been separately studied for more than two decades, are actually linked via the Rho-Pol II CTD code signaling shortcut. This shortcut mode of transcriptional control has an advantage of rapidly bringing about large scale transcriptional changes. Adopting this transcriptional mode enables eukaryotes to robustly respond to internal cues and external stimuli, and thus increases their environmental fitness.

 

OSU1-mediated C/N balance signaling Cellular C and N metabolism must be tightly coordinated to sustain optimal plant growth and development at the molecular and whole plant systems levels. Furthermore, C/N balance is also critical for the ecosystem response to elevated atmospheric CO2. Despite numerous physiological and molecular studies in C/N balance or ratio response, very few genes have been shown to play important roles in C/N balance signaling.

 

Using a genetic approach, we have identified a novel gene (OVERSENSITIVE TO SUGAR1, OSU1) involved in C/N balance response in Arabidopsis thaliana (Gao et al., 2008). Mutations in the OSU1 gene result in the hypersensitivity of the seedlings to the imbalanced C/N (high C/low N, and low C/high N), but the osu1 mutants respond normally as wild-type under the balanced C/N, low C/low N and high C/high N. OSU1 encodes a putative AdoMet-dependent methyltransferase. Interestingly, osu1 mutants are allelic to qua2/tsd2, the cell-adhesion-defective mutants reported by two other groups (Mouille et al., 2007; Krupkova et al., 2007). This indicates that OSU1/QUA2/TSD2 might either have distinct substrates in the control of cell adhesion and C/N balance response or is important in linking cell wall biogenesis and C/N balance response. We are currently investigating its signaling mechanisms in the C and N nutrient balance response.

 

S nutrient sensing and C-N-S cross-talk  Through a C, N and S combinatorial design, we have revealed that activation of a vacuolar sulphate transporter gene (SULTR4;2) and a putative b-glucosidase 28 (BGLU28) gene by S deficiency is primarily dependent on the C availability which interacts synergistically with N (Dan et al., 2007). This demonstrates the differential effects of C, N and S nutrients on gene expression. To understand the regulatory mechanism, we have taken advantage of this novel nutrient regulatory pattern to identify nutrient sensing/signaling proteins involved in the C-N-S cross-talk. Genetic, physiological and molecular approaches will be used to understand how plants sense the nutrient status and cross-talk to optimize the opportunity for cellular metabolism, growth and development.

 

Using the BGLU28:GUS reporter-based mutant screen, we have identified two novel alleles (sel1-15 and sel1-16) of the Arabidopsis high affinity transporter SULTR1;2 in which sulfate uptake was inhibited and gene expression was enhanced (Zhang et al., 2014). However, the sensitivity in sulfur-induced down-regulation for several genes known to affect S nutrient response was reduced in sel1-15 and sel1-16 alleles even if the internal S status was similar between wild-type and the mutant alleles. This genetic evidence indicates that SULTR1;2 has a dual role in sulfate transport and sensing, which may be classified as a transporting receptor or “transceptor”. We are currently working on the mechanism by which SULTR1;2 senses the sulfur nutrient status and how this signal is transmitted to the nucleus. One of the intriguing features of SULTR1;2 is that G208, which is mutated to D208 in sel1-16, is located on transmembrane helix 5 (TM5) and is highly conserved among all transporters related to SULTR1;2 from plants to yeast and animals (Zheng et al., 2014).

 

Applied research: Systems biology analysis of citrate metabolic regulation and genetic improvement of fruit acidity in orange and strawberry  Citrate is an important organic acid involved in the determination of fruit acidity and thus sweetness for many climacteric (such as tomato and apple) and non-climacteric fruits (such as citrus and strawberry). Through collaboration with Citrus Research Institute of Southwest University, we have used an integrated systems biology approach to analyze fruit acidity control gene networks (Huang et al., 2016). We are currently testing the functions of those hub genes using genetic approaches in sweet orange and strawberry.

 

 

Selected Publications

 

  

[15] Zhang B, Yang G, Chen Y, Zhao Y, Gao P, Liu B, Wang H and Zheng Z-L  (2016)

C-terminal domain (CTD) phosphatase links Rho GTPase signaling to Pol II CTD phosphorylation in Arabidopsis and yeast.

Proc. Natl. Acad. Sci. U.S.A. 113: doi: 10.1073/pnas.1605871113 [Supporting Information]

 

[14] Huang D, Zhao Y, Cao M, Qiao L and Zheng Z-L (2016)

Integrated systems biology analysis reveals candidate genes for acidity control in developing fruits of sweet orange (Citrus sinensis L. Osbeck).

Frontiers in Plant Science 7: 486

 

[13] Zheng Z-L, Zhang B and Leustek T (2014)  

Transceptors at the boundary of nutrient transporters and receptors: A new role for Arabidopsis SULTR1;2 in sulfur sensing.

Frontiers in Plant Science 5:710

 

[12] Zhang B, Pasini R, Dan H, Joshi N, Zhao Y, Leustek T and Zheng Z-L (2014)

Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulfate transporter in response to sulfur nutrient status.

Plant Journal 77:185-197

 

[11] Zheng Z-L and Zhao Y (2013)

Transcriptome comparison and gene coexpression network analysis provide a systems view of citrus response to ‘Candidatus Liberibacter asiaticus’ infection.

BMC Genomics 14: 27

 

[10] Zheng Z-L (2009)

Carbon and nitrogen nutrient balance signaling in plants.

Plant Signaling & Behavior 4: 584-591

 

[9] Xin Z, Wang A, Yang G, Gao P and Zheng Z-L (2009)

The Arabidopsis A4 subfamily of lectin receptor kinases negatively regulates abscisic acid response in seed germination.

Plant Physiology 149: 434-444

 

[8] Gao P, Xin Z and Zheng Z-L (2008)

The OSU1/QUA2/TSD2-encoded putative methyltransferase is a critical modulator of carbon and nitrogen nutrient balance response in Arabidopsis.

PLoS ONE 3: e1387

 

[7] Yang G, Gao P, Zhang H, Huang S and Zheng Z-L (2007)

A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 GTPase in Arabidopsis.

PLoS ONE 2: e1074

 

[6] Dan H, Yang G and Zheng Z-L (2007)

A negative regulatory role for auxin in sulphate deficiency response in Arabidopsis thaliana.

Plant Molecular Biology 63: 221-235

 

[5] Xin Z, Zhao Y and Zheng Z-L (2005)

Transcriptome analysis reveals specific modulation of abscisic acid signaling by ROP10 small GTPase in Arabidopsis.

Plant Physiology 139: 1350-1365

 

[4] Fu Y, Gu Y, Zheng Z-L, Wasteneys G and Yang Z (2005)

Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis.

Cell 120: 687-700

 

[3] Zheng Z-L, Nafisi M, Tam A, Li H, Crowell DN, Chary SN, Shen J, Schroeder JI and Yang Z (2002)

Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis.

Plant Cell 14: 2787-2797

 

[2] Li H, Shen J, Zheng Z-L, Lin Y and Yang Z (2001)

The Rop GTPase switch controls multiple developmental processes in Arabidopsis.

Plant Physiology 126: 670-684

 

[1] Zheng Z-L, Yang Z, Jang J-C and Metzger JD (2001)

Modification of plant architecture in chrysanthemum by ectopic expression of the tobacco phytochrome B1 gene.

Journal of the American Society for Horticultural Sciences 126: 19-26  (Won the American Society for Horticultural Sciences Most Outstanding Publication Award of 2001)