Mechanistic dissection of signal transduction strategies in plant and understanding the molecular and cellular processes that underlie male-female interaction and polarized cell growth in plant reproduction

Background and Training

PhD: Yale University

Postdoctoral training: Harvard University

Research Summary

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.

Publications (2021-2024)

  • Zhong S, Zhao P, Peng X, Li H-J, Duan Q, Cheung AY. (2024) From gametes to zygote: mechanistic advances and emerging possibilities in plant reproduction. Plant Physiology, ASPB Centennial Celebration Issue. In press.
  • Cheung AY. (2024) FERONIA: A receptor kinase at the core of a global signaling network.  Annu. Rev. Plant Biol. 75, In press.
  • Liu M-C J, Yeh F-L J, Yvon R, Simpson K, Chambers J, Wu H-M, Cheung AY. (2024) Extracellular pectin-RALF peptide phase separation mediates FERONIA global signaling function.  Cell 187, 312-330. Published online, December 28, 2023.
  • Huang J, Yang L, Zhang L, Zhao Y, Yang L, Wu X, Hui J, Cui X, Yang H, Liu S, Xu Q,  Pang M, Cao Y, Xu G, Chen Y, Ren X, Lv J, Yu J, Ding J, Wang N, Wei X, Lin Q, Yuan Y, Zhang X, Ma C, Cheng, Dai C, Wang P, Wang Y, Cheng F, Zeng W, Palanivelu R, Wu H-M, Zhang X, Cheung AY (co-corresponding), Duan Q. (2022) Stigma receptors control intra– and interspecies barriers in Brassicaceae. Nature Jan. 25 2023 online. doi: 10.1038/s41586-022-05640-x
  • Liu H, Huang J, Zhang X, Liu G, Liang W, Zhu G, Dong M, Li M, Zhang J, Yang W, Xiao W, Cheung AY, Tao L-Z. (2023) The rice RAC/ROP GTPase Activator OsRopGEF10 functions in crown root development by regulating cytokinin signaling.  The Plant Cell 35, 453-468. doi: 10.1093/plcell/koac297
  • Noble JA, Bielski NV, Liu, M-C J, DeFalco TA, Stegmann M, Nelson ADL, McNamara K, Sullivan S, Dinh KK, Khuu N, Hancock S, Shiu S-H, Zipfel C, Cheung AY, Beilstein MA, Palanivelu R. (2022). Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization. Plant Physiol 190, 2539-2556. 10.1093/plphys/kiac444
  • Cheung AY, Duan Q-h, Li C, Liu M-D J, Wu H-M. (2022) Pollen-pistil interactions: it takes two to tangle but a molecular cast of many to deliver. Curr Opin Plant Biol doi: 10.1016/j.pbi.2022.102279.
  • Zhong S, Li L, Wang Z, Ge Z, Li Q, Bleckmann A, Wang J, Song, Z, Shi Y, Liu T, Li L, Zhou H, Wang Y, Zhang L, Wu H-M, Lai L, Gu H, Dong J, Cheung AY, Dresselhaus T, Qu L-j. (2022) RALF peptide signaling controls the polytubey block in Arabidopsis. Science 375, 290-296.  doi: 10.1126/science.abl4683
  • Cheung AY, Cosgrove D, Hara-Nishimura I, Jurgens G, Llyod C, Robinson DG, Staehelin LA.  (2022) A rich and bountiful harvest – Key discoveries in Plant Cell Biology. Plant Cell online Setp. 2021. Doi: 10.1093/plcell/koab234
  • (An invited collective article on plant cell biology breakthroughs in the past decades for a focus issue on Plant Cell Biology, January 2022)
  • Yang H, Wang D, Guo L, Pan H, Yvon R, Garman S, Wu H-M, Cheung AY. (2021) Malectin/Malectin-domain-containing proteins: A repertoire of cell surface molecules with broad functional potential. The Cell Surface 7.
  • Zhang L, Huang J, Su S, Wei X, Yang, L, Zhao H, Yu J Wang J, Hui J, Hao, S, Song S, Cao Y, Wang M, Zhang X, Zhao Y, Wang Z, Zeng W, Wu H-M, Yuan Y, Cheung AY, Duan Q. 2021. FERONIA-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa. Current Biology (May 18, 2021);  doi: 10.1016/j.cub.2021.04.060.  
  • Liu C, Shen L, Xiao Y, Vyshedsky D, Peng C, Sun X, Liu Z, Cheng L, Zhang H, Han Z, Chai J, Wu H-M, Cheung AY, Li C. 2021. Pollen PCP-B peptides unlock a stigma peptide-receptor kinase gated mechanism for pollination.  Science 372, 171-175. doi: 10.1126/science.abc6107. PubMed PMID: 33833120.

Selected Publications Prior To 2021

  • Cheung AY, Qu L-j, Russinova J, Zhao Y, Zipfel C. Focus Issue on Receptors and Signaling. Plant Physiol. April Issue.
  • Duan Q-h, Liu M-CJ, Kita D, Jordan S, Yeh F-LJ, Yvon R, Carpenter H, Federico AN, 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
  • 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.
  • Feng W, Kita D, Peaucelle A, Doan V, Duan Q-h, Liu M-C, Maman J, Yvon R, 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 Z, Bergonci T, 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
  • 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 Physiol175, 157-171. doi:10.1104/pp.17.00697.
  • 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
  • Li C, Yeh F-L, Cheung AY, Duan Qh, Kita D, Liu M-C, Maman J, Luu EJ, Wu BW, Gates L, Jalal M, Kwong A, Carpenter H, Wu H-M. 2015. Glycosylphosphatidylinositol-anchored proteins act as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife4:e06587. doi:
  • 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 L, 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]
  • 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]
  • 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