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Steve Briggs

Research

Mating between genetically distinct parents can produce heterosis, providing their progeny with remarkable increases in fitness. Heterosis is the difference in vigor between a hybrid and its parents. Vigor is measured many ways including as growth, stress resistance, and reproductive advantage. The phenomenon of heterosis was first described by Charles Darwin and it occurs in all eukaryotes where it has been examined. Heterosis in crops and livestock increases many traits far above the levels of either parent, including biomass and harvestable grain for maize, the plant we mostly study. Breeding hybrids requires expensive and lengthy tests to first develop new inbred parents and then to test combinations of parents to make new hybrids. Despite its importance in agriculture, the changes in physiology that cause heterosis remain obscure. Progress in maize breeding has not substantially increased the amount of heterosis. It is unclear whether improvements in heterosis are possible and yet have lagged because breeders lack biomarkers or an understanding of heterosis.

Using high-precision peptide mass spectrometry combined with RNA-seq, we found that one inbred parent of a hybrid has higher levels of key protein complexes than the other parent, and these complexes are over-expressed in the hybrid. In other words, these complexes display proteome dominance; their transcripts do not follow this pattern. The protein complexes contain subunits encoded by both the plastid genome and the nuclear genome and include those required for protein synthesis and for the light reactions of photosynthesis. Levels of the plastid ribosome in laboratory-grown seedling leaves are quantitatively predictive of trait heterosis in adult, field-grown plants. The molecular differences between inbreds and their hybrid resemble the differences between early and late leaf maturation. The results suggest that heterosis increases the rate or extent of organ maturation. We observed that expression levels of biosynthesis genes for the stress hormone ethylene (ET), including ACS transcripts, are repressed in hybrids. The hybrid-specific differences in expression levels for ribosome and photosynthesis proteins were recreated in an inbred that contained mutated ACS genes. Repression of ET levels in Arabidopsis hybrids has been previously reported. Thus, our findings indicate that heterosis physiology may be at least partially conserved between monocots and dicots.

An unsupervised network analysis showed that over-expression of digenomic proteins in hybrids is associated with elevated levels of proteostasis elements including chloroplast chaperones and protein complex assembly factors. We are exploring whether these proteostasis elements cause the increased levels of digenomic protein complexes. In contrast, inbreds display elevated levels of ERAD and UPR indicating they are experiencing proteostasis stress. Our focus, therefore, is on the relationship between proteostasis and heterosis.

Select Publications

  • Walley JW, Shen Z, McReynolds MR, Schmelz EA, Briggs SP. Fungal-induced protein hyperacetylation in maize identified by acetylome profiling. Proc Natl Acad Sci U S A. Jan 2;115(1):210-215. doi:10.1073/pnas.1717519115. Epub 2017 Dec 19. PMID: 29259121
  • Mafu S, Ding Y, Murphy KM, Yaacoobi O, Addison JB, Wang Q, Shen Z, Briggs SP, Bohlmann J, Castro-Falcon G, Hughes CC, Betsiashvili M, Huffaker A, Schmelz EA, Zerbe P. Discovery, Biosynthesis and Stress-Related Accumulation of Dolabradiene-Derived Defenses in Maize. Plant Physiol. Apr;176(4):2677-2690. doi: 10.1104/pp.17.01351. Epub 2018 Feb 23. PMID: 29475898
  • Lacal Romero J, Shen Z, Baumgardner K, Wei J, Briggs SP, Firtel RA. The Dictyostelium GSK3 kinase GlkA coordinates signal relay and chemotaxis in response to growth conditions. Dev Biol. Mar 1;435(1):56-72.doi: 10.1016/j.ydbio.2018.01.007. Epub 2018 Jan 20. PMID: 29355521
  • Hasan MK, Yu J, Widhopf GF 2nd, Rassenti LZ, Chen L, Shen Z, Briggs SP, Neuberg DS, Kipps TJ. Wnt5a induces ROR1 to recruit DOCK2 to activate Rac1/2 in chronic lymphocytic leukemia. Blood. Jul 12;132(2):170-178. doi: 10.1182/blood-2017-12-819383. Epub 2018 Apr 20. PMID: 29678828May 3. PMID: 28465528
  • Hasan MK, Yu J, Chen L, Cui B, Widhopf Ii GF, Rassenti L, Shen Z, Briggs SP, Kipps TJ. Wnt5a induces ROR1 to complex with HS1 to enhance migration of chronic lymphocytic leukemia cells. Leukemia. Dec;31(12):2615-2622. doi: 10.1038/leu.2017.133. Epub 2017 May 3. PMID: 28465529
  • Marcon C, Malik WA, Walley JW, Shen Z, Paschold A, Smith LG, Piepho HP, Briggs SP, Hochholdinger F. A high resolution tissue-specific proteome and phosphoproteome atlas of maize primary roots reveals functional gradients along the root axis. Plant Physiol. 2015 Mar 16. pii: pp.00138.2015
  • Yu J, Chen L, Chen Y, Hasan MK, Ghia EM, Zhang L, Wu R, Rassenti LZ, Widhopf GF, Shen Z, Briggs SP, Kipps TJ. Wnt5a induces ROR1 to associate with 14-3-3ζ for enhanced chemotaxis and proliferation of chronic lymphocytic leukemia cells. Leukemia. Dec;31(12):2608-2614. doi: 10.1038/leu.2017.132. Epub 2017 May 3. PMID: 28465528
  • Wang JZ, Li B, Xiao Y, Ni Y, Ke H, Yang P, de Souza A, Bjornson M, He X, Shen Z, Balcke GU, Briggs SP, Tissier A, Kliebenstein DJ, Dehesh K. Initiation of ER Body Formation and Indole Glucosinolate Metabolism by the Plastidial Retrograde Signaling Metabolite, MEcPP. Mol Plant. Nov 6;10(11):1400-1416. doi:10.1016/j.molp.2017.09.012. Epub 2017 Sep 28. PMID: 28965830
  • Walley JW, Sartor RC, Shen Z, Schmitz RJ, Wu KJ, Urich MA, Nery JR, Smith LG, Schnable JC, Ecker JR, Briggs SP. Integration of omic networks in a developmental atlas of maize. Science. Aug 19;353(6301):814-8. doi: 10.1126/science.aag1125. PMID: 27540173
  • Khanna A, Lotfi P, Chavan AJ, Montaño NM, Bolourani P, Weeks G, Shen Z, Briggs SP, Pots H, Van Haastert PJ, Kortholt A, Charest PG. The small GTPases Ras and Rap1 bind to and control TORC2 activity. Sci Rep. May 13;6:25823. doi: 10.1038/srep25823. PMID: 27172998
  • Yu J, Chen L, Cui B, Widhopf GF 2nd, Shen Z, Wu R, Zhang L, Zhang S, Briggs SP, Kipps TJ. Wnt5a induces ROR1/ROR2 heterooligomerization to enhance leukemia chemotaxis and proliferation. J Clin Invest. Feb;126(2):585-98. PMID: 26690702
  • Huang H, Alvarez S, Bindbeutel RK, Shen Z, Naldrett MJ, Evans BS, Briggs SP, Hicks LM, Kay SA, Nusinow DA. Identification of evening complex associated proteins in Arabidopsis by affinity purification and mass spectrometry. Mol Cell Proteomics. Jan;15(1):201-17. doi: 10.1074/mcp.M115.054064. Epub 2015 Nov 6. PMID: 26545401
  • Marcon C, Malik WA, Walley JW, Shen Z, Paschold A, Smith LG, Piepho HP, Briggs SP, Hochholdinger F. A high-resolution tissue-specific proteome and phosphoproteome atlas of maize primary roots reveals functional gradients along the root axes. Plant Physiol. May;168(1):233-46. doi: 10.1104/pp.15.00138. Epub 2015 Mar 16. PubMed PMID: 25780097; PubMed Central PMCID: PMC4424028.
  • Yu J, Chen L, Cui B, Widhopf GF 2nd, Shen Z, Wu R, Zhang L, Zhang S, Briggs SP, Kipps TJ. Wnt5a induces ROR1/ROR2 heterooligomerization to enhance leukemia chemotaxis and proliferation. J Clin Invest. Dec 21. pii: 83535. doi: 10.1172/JCI83535.
  • Nakasaki M, Hwang Y, Xie Y, Kataria S, Gund R, Hajam EY, Samuel R, George R, Danda D, M J P, Nakamura T, Shen Z, Briggs S, Varghese S, Jamora C. The matrix protein Fibulin-5 is at the interface of tissue stiffness and inflammation in fibrosis. Nat Commun. Oct 15;6:8574. doi: 10.1038/ncomms9574.
  • Pineda G, Shen Z, Ponte de Albuquerque C, Reynoso E, Chen J, Tu C-C, Tang W, Briggs S, Zhou H, Wang JY. Proteomics Studies of the Interactome of RNA Polymerase II C-Terminal Repeated Domain. BMC Research Notes Oct 29;8:616. doi: 10.1186/s13104-015-1569-y
  • Walley J, Xiao Y, Wang J-Z, Baidoo EE, Keasling JD, Shen Z, Briggs SP, Dehesh K. Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. Proc Natl Acad Sci USA April 28, doi: 10.1073/pnas.1504828112
  • Xiong J, Todorova D, Su NY, Kim J, Lee PJ, Shen Z, Briggs SP, Xu Y. Stemness factor Sall4 is required for DNA damage response in embryonic stem cells. J Cell Biol. Mar 2;208(5):513-20. doi: 10.1083/jcb.201408106.
  • Chaudhary R, Atamian HS, Shen Z, Briggs SP, Kaloshian I. Potato aphid salivary proteome: enhanced salivation using resorcinol and identification of aphid phosphoproteins. J Proteome Res. Apr 3;14(4):1762-78. doi: 10.1021/pr501128k.

Biography

Briggs earned his Ph.D. from Michigan State University and spent the first half of his career in industry as Director at Pioneer/DuPont; President of Torrey Mesa Research Institute; and Senior Vice President for Corporate Research at Diversa. He served as Senior Staff Investigator at Cold Spring Harbor Laboratory. Briggs joined the faculty at UCSD as Professor where he served as Chair of the Section of Cell & Developmental Biology, Associate Dean of the Division of Biology, and Interim Chair of the Department of Chemistry and Biochemistry. He is a member of the National Academy of Sciences, a Fellow of the American Association for the Advancement of Science, and a Fellow of the National Academy of Inventors.

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