PhD: Yale University
Postdoctoral training: Harvard University
Our overall research interest is in understanding signaling strategies in plants that support growth and reproduction. A focus area of our work is in understanding the cell-cell communicative processes between male (pollen)-female (pistil) that lead to fertilization. Another focus area is in deciphering signal transduction mechanisms that have general impacts on plant growth and development. While our research spans the early seedling and the mature flowering stages of the life cycle of a plant, we focus on common regulatory nodes, mediated by RAC/ROPs (plant RHO GTPases), polarized pollen tube and root hair growth as our main experimental systems.
Our research utilizes cell biological, biochemical, molecular, and more recently biophysical approaches. Over the years, our efforts have elucidated cellular mechanisms that regulate polarized cell growth and molecular mechanisms with broad biological significances. Our recent work focuses on a family of receptor kinases, here referred to as the FERONIA-BUPS family, names of the key female and seedling-expressed member (FERONIA) and a cell surface receptor for RAC/ROPs, and its pollen-expressed counterparts (BUPS).
In reproduction, pollen tubes grow in the pistil to transport the sperm to the egg chamber (female gametophyte) inside the ovules. Pollen tube growth is driven by the pollen cytoplasm but is regulated by signals that originate from the female tissues to nourish and guide them to enter the female gametophyte. Then the pollen tube bursts to release sperm and enables fertilization, while mechanisms are activated to prevent further pollen tube entrance to prevent polyspermy, which ensure progeny health and maximize reproductive yield (seed production). Our efforts are centered on identifying female signal molecules, their receptors on the pollen surface, the pollen components that relate these signals, drive and regulate the polarized cell growth machinery, and also mechanisms that control sperm delivery and the prevention of polyspermy. Our current work largely surrounds processes regulated by FERONIA-BUPS and additional homologs expressed in pollen and pistillate cells. Our goal is to gain a comprehensive understanding of pollen-pistil interactions starting from pollen germination on the pistil receptive surface, the long distance and local regulation of pollen tube guidance till sperm delivery for fertilization.
Our work in plant growth development mainly takes advantage of the relatively facile seedling growth process (compared with reproduction) to decipher signal transduction mechanisms. Our current work has evolved from an earlier interest in RAC/ROP-mediated auxin signaling to the current focus on understanding how diverse growth-regulatory signaling pathways are coordinated. Our efforts led to the discovery of a key co-receptor complex comprised of FERONIA and a glycosylphosphatidylinositol-anchored protein (LLG1) that has almost global impact on plant growth and survival. Building from this, we now focus on elucidating how FERONIA-LLG1 achieves its global signaling role.
We welcome inquiry from prospective graduate students and postdocs to join us; we also welcome undergraduate participants in our research.
*corresponding; 1co-first author; uundergraduate
Cheung AY, Qu L-j, Russinova J, Zhao Y, Zipfel C. Focus Issue on Receptors and Signaling. Plant Physiol. April Issue.
Duan Q-h1, Liu M-CJ1, Kita D, Jordan S, Yeh F-LJ, Yvon R, Carpenter H, Federico ANu, Garcia-Valencia L, Eyles SJ, Wang C-S, Wu H-M, Cheung AY*. FERONA controls pectin- and nitric oxide-mediated male-female interaction. Nature, 579, 561-566. doi: 10.1038/s41586-020-2106-2.
Zhao P, Zhou X-m, Zhao L-l, Cheung AY, Sun M-X. Autopathy-mediated compartmental cytoplasmic deletion is essential for tobacco pollen germination and male fertility. January 30, 2020, Autophagy, doi: 10.1080/15548627.2020.1719722
Cheung AY*. To live, or not to live, that is the question. Current Biology, 29, R1174-R1178 (A Commentary). doi: 10.1016/j.cub.2019.09/057
Ge Z, Zhao Y, Liu M-C, Wang L, Zhong S, Hou S, Jian J, Liu T, Huang Q, Xiao J, Gu H, Wu H-M, Dong J, Dresselhaus T, Cheung AY, Qu L-J. LLG2/3 are co-receptors in BUPS/ANX-RALF signaling to regulate Arabidopsis pollen tube integrity. Current Biology 29, 3256-3265. doi: 10.1016/j.cub.2019.08.032.
Soares A, Niedermaier S, Faro R, Loos A, Manadas B, Faro C, Huesgen P, Cheung AY*, Simoes I. An atypical aspartic protease modulates lateral root development in Arabidopsis thaliana. J. Exp. Bot. 70, 2157-2171. doi: 10.1093/jxb/erz059
Ge Z, Cheung AY, Qu L-J. Pollen tube integrity regulation in flowering plants: insights from molecular assemblies on the pollen tube surface. New Phytoplogist 222, 687-693. [A review]. doi: 10.1111/nph
Duan Q-h, Cheung AY*. Context-specific dependence on FERONIA kinase activity. FEBS Lett 592: 2392-2394. [A Commentary]. doi: 10.1002/1873-3468
Feng W, Kita D, Peaucelle A, Doan Vu, Duan Q-h, Liu M-C, Maman J, Yvon Ru, Steinhorst L, Schmitz-Thom I, Cartwrigh HN, Kudla J, Wu H-M, Cheung AY*, Dinneny JD. The FERONIA receptor kinase maintains cell wall integrity during salt stress through Ca2+ signaling. Current Biology 28, 666-675. doi: 10.1016/j.cub.2018.01.023
Ge Z1, Bergonci T1, Zhao Y, Zou Y, Du S, Liu M-C, Luo X, Ruan H, García-Valencia LE, Zhong S, Hou S, Huang Q, Lai L, Moura DS, Gu H, Dong J, Wu H-M, Dresselhaus T, Xiao J, Cheung AY*, Qu L-J. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358, 1596-1600. doi: 10.1126/science.aao3642
Garcia-Valencia LE, Bravo-Alberto CE, Wu H-M, Rodriguez-Sotres R, Cheung AY, Cruz-Garcia F. 2017 SIPP, a novel mitochondrial phosphate carrier mediates self-incompatibility. Plant Physiol. 175, 1105-1120. doi:10.1104/pp.16.01884
Liu Y, Dong Q, Kita D, Liu G, Wu X, Zhu X, Cheung AY, Wu H-M, Tao L-z. 2017.RopGEF1 plays a critical role in polar auxin transport in early development. Plant Physiol. 175, 157-171. doi:10.1104/pp.17.00697.
Padmanaban S, Czerny DD, Levin K, Leydon RR, Su RT, Maugel TK, Zou YJ, Chanroj S, Cheung AY, Johnson MA, Sze, H. 2017. Transporters involved in pH and K+ homeostasis affect pollen wall formation, male fertility and embryo development. J. Exp. Bot. 68, 3165-3178. doi:10.1093/jxb/erw483
Cheung AY, Amasino R, Dresselhaus T, Kuhlemeier C. 2017. Focus Issue Flowering and Reproduction. Plant Physiol. January Issue.
Li C, Wu H-M, Cheung AY*. FERONIA and her pals: functions and mechanisms. Plant Physiol 171, 2379-2391 [A Review]. doi: 10.1104/pp.16.00667
Cheung AY*, Wu, H-M. LURE is bait for multiple receptors. Nature 531, 178-180. [News and Views]. doi: 10.1038/531178a
Cheung, AY*, Wu, H-M. 2015. Stomato Patterning:Serks putting the mouths in their right place. Curr. Biol. 25, R827-844. [A Commentary]. doi: 10.1016/j.cub. 2015.08.049
Li C, Yeh F-L, Cheung AY*, Duan Qh, Kita D, Liu M-C, Maman Ju, Luu EJu, Wu BWu, Gates Lu, Jalal Mu, Kwong Au, Carpenter Hu, Wu H-M. 2015. Glycosylphosphatidylinositol-anchored proteins act as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife, 4:e06587. doi:http://dx.doi.org/10.7554/eLife.06587
Cheung AY*, Li C, Zou YJ, Wu HM. 2014. Glycosylphosphatidylinositol anchoring: control through modification. Plant Physiol. 166, 748-750. doi: http://dx.doi.org/10.1104/pp.114.246926 [PubMed]
Huang JB, Liu H, Chen M, Li X, Wang M, Yang Y, Wang C, Huang J, Liu G, Xu J, Cheung AY, Tao L-z. 2014. ROP3 GTPase contributes to polar auxin transport and auxin responses and is important for embryogenesis and seedling growth in Arabidopsis. Plant Cell 26, 3501-3518. doi: http://dx.doi.org/10.1105/tpc.114.127902 [PubMed]
Duan Q, Kita D, Johnson EA, Aggarwal M, Gates Lu, Wu H-M, Cheung AY*. 2014. Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nature Commun. 5, 3129 doi:10.1038/ncomms4129. [PubMed]
Hernandez A, Quito C, Johnson EA, Wu H-M, Cheung AY, Cardenas L. 2013. Using Hyper as a molecular probe to visualize hydrogen peroxide in living plant cells: a method with virtually unlimited potential in plant biology. Methods in Enzymology 527, 275-290. doi: 10.1016/B978-0-12-405882-8.00015-5 [PubMed]
Wang H, Zhuang X, Cai Y, Cheung AY, Liwen J. 2013. Apical F-actin regulated exocytic targeting of NtPPMEI1 is essential for pollen tube cell wall construction and rigidity. Plant J. 76, 367-379. doi: 10.1111/tpj.12300
Nibau C, Tao L-z, Levasseur Ku, Wu H-M, Cheung AY*. 2013. The Arabidopsis small GTPase AtRac7/ROP9 is a modulator of auxin and ABA signaling. J. Exp. Bot. 64, 3425-3437. doi:10.1093/jxb/ert179 [PubMed]
Chen CY, Zheng W-G, Wu H-M, Cheung AY*. 2013. Pollen germination activates theapical membrane located RAC/ROP GTPase switch. Molecular Plant 6, 1358-1361. doi: 10.1093/mp/sst074. doi: 10.1093/mp/sst074
Wu H-M, Cheung AY*, 2011. THESEUS and relatives: cell wall-sensing receptor-like kinases. Curr. Opin. Plant Biol. 14, 632-641. doi: 10.1016/j.pbi.2011.09.001
Chen M, Liu H, Kong X, Zhang N, Yang Y, Li R, Yue J, Chen D, Tian R, Li C, Cheung AY, Tao L-z. 2011. The RopGEF7 is required to control Plethora (PLT)-dependent maintenance of root stem cell niche in Arabidopsis. The Plant Cell 23, 2880-2894.
Wu H-M, Hazak O, Cheung AY*, Yalovsky S. 2011. RAC/ROP GTPases and Auxin Signaling. The Plant Cell 23, 1208-1218. [A review] doi: 10.1105/tpc.111.083907
Lu Y, Chanroj S, Zulkifli L, Johnson M, Uozumi N, Cheung AY, Sze, H. Pollen Tubes Lacking a Pair of K+ Transporters Fail to Target Ovules in Arabidopsis. 2011. The Plant Cell, 23, 81-93. doi: 10.1105/tpc. [PubMed]
Wang H, Zhuang X, Cai Y, Cheung AY, Liwen J. (2013) Apical F-actin regulated exocytic targeting of NtPPMEI1 is essential for pollen tube cell wall construction and rigidity. Plant J. 76, 367-379. doi: 10.1111/tpj.12300
Nibau C, Di Stilio VS, Wu H-M, Cheung AY*. 2010. Arabidopsis and Tobacco superman regulate hormone signalling and mediate cell proliferation and differentiation. 2010. J Exp Bot 62, 949-961. doi: 10.1093/jxb/erq325 [PubMed]
Duan Q, Kita D, Li C, Cheung AY*, 2010. Wu H-M. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Nat'l Acad. Sci. USA 2010, 107: 17821-17826. doi: 10.1073/pnas.1005366107 [PubMed]
Cheung AY*, Boavida L, Aggarwal M, Wu H-M, Feijo J*. 2010. The Pollen Tube Journey in the Pistil and Imaging the In Vivo process by two-Photon Microscopy. J. Exp. Bot. 2010, 61:1907-1915. doi: 10.1093/jxb/erq062. [PubMed]
Cheung AY*, Niroomand S, Zou Y, Wu H-M. 2010. A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc. Natl. Acad. Sci. USA. 107, 16390-16395. doi: 10.1073/pnas.1008527107