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Steve Briggs

Research

Plants, animals, and humans display inbreeding depression associated with increased genetic uniformity and characterized by reduced vigor. Mating between genetically distinct inbred parents can produce hybrid vigor, or heterosis, defined as the difference in vigor between a hybrid and 1) the average of its parents or 2) the better-performing parent. Hybrids may outperform their parents in terms of size, vigor, yield, abiotic and biotic stress resistance, longevity, and reproductive advantage. Maize is the most productive crop, and it was the first hybrid crop to be made and sold. Heterosis in maize increases many traits far above the levels of the higher parent, including biomass and harvestable grain. Despite its importance in agriculture, the changes in physiology that cause hybrid vigor remain obscure. Breeding hybrids requires expensive and labor intensive field tests of both the hybrids and their parents. Progress in maize breeding has greatly improved yield through increased tolerance of high-density planting stress, and this primarily constitutes the non-heterosis portion of yield. It is unclear whether substantial improvements in heterosis are possible and yet have lagged because breeders lack seedling biomarkers for adult plant heterosis.

We study inbreeding depression and its relief by hybridization to produce heterosis. Our primary system is maize and our primary tool is peptide mass spectrometry. We use network analyses and machine learning to interrogate large datasets. At the outset of our studies, the field of heterosis lacked a clear description of the key differences in physiology that distinguish hybrids from their less vigorous inbred parents. The field also lacked an evidence-based hypothesis for the mechanism of heterosis, which gives rise to the robust physiology of hybrids. Our most recent articles provide explanations for some of the advantages in physiology that are associated with heterosis. We found that maize hybrids selectively over-express protein complexes containing subunits encoded by both the plastid genome and the nuclear genome. These plastid digenomic protein complexes include those required for photosynthesis and protein synthesis. Over-expression was associated with elevated levels of nuclear-encoded sigma factors that regulate transcription of the plastid genome, and with repressed levels of nuclear-encoded ethylene biosynthetic enzymes. Levels of the plastid ribosome in seedling leaves are quantitatively predictive of the levels of trait heterosis in adult, field-grown plants. Accordingly, we can for the first time use seedling protein expression levels to predict adult plant heterosis levels. The molecular differences between inbreds and their hybrid resemble the differences between early and late leaf maturation. This observation was made using both seedling and mature leaves and it was critical to apply proteomics as the differences are more pronounced for protein abundance than transcript abundance. The results suggest that heterosis increases the rate or extent of organ maturation. We observed that expression levels of ethylene (ET) biosynthesis genes, including ACS transcripts, were repressed in hybrids. The hybrid-specific differences in photosynthesis and ribosome protein expression levels were recreated in an inbred that contained mutated ACS genes. Therefore, repression of ET biosynthetic enzyme levels is upstream of the heterosis molecular phenotypes. 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.

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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