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Gene Expression

Head of Group: Professor Sir David Baulcombe

Regius Professor of Botany and Edward Penley Abraham Royal Society Research Professor

david baulcombe

Understanding the growth, development, physiology and evolution of plants depends on knowing how genes are switched on and off. Progress in crop improvement relies similarly on having unravelled networks of genetic regulation. To shed light on these processes we investigate interspecific hybrids and disease resistance in tomato.

tomatoes

The unifying themes in these projects derive from previous discoveries in small regulatory RNA, epigenetics and the mechanisms of disease resistance in plants. An overview of these past discoveries is described in David Baulcombe's brief memoir entitled "Normal Botany"

Current projects include:

Disease and disease resistance

Our earlier research into disease and disease resistance had two separate strands based on RNA and protein based mechanisms. In our RNA work we discovered small interfering (si)RNAs with many diverse roles including anti-viral defense. The protein work focused on innate immunity proteins with nucleotide binding sites and leucine rich repeats (NLRs). We demonstrated how the domains of these proteins may interact intra-molecularly (Moffett et al, 2002), how these proteins interact inter-molecularly with each other (Peart et al, 2005) and how they can be evolved artificially to have novel disease resistance specificity (Farnham & Baulcombe, 2006; Harris et al, 2013).

A recent finding brings these two strands together because NLR mRNAs are regulated by a cascade involving siRNAs (Shivaprasad et al, 2012a). If this cascade is blocked we can enhance quantitative disease resistance to Phytophthora infestans (an oomycete) and Pseudomonas syringae (a bacterium)(Canto-Pastor et al, 2019).

tomato leaves
Three tomato leaves inoculated with P. infestans and illuminated under UV light. The disease lesions are dark regions and they are larger in control plants than in plants with a blocked RNA silencing cascade.

Interspecific hybrids

Our earlier discovery of a link between siRNA and epigenetics (Herr et al, 2005) prompted the hypothesis to explain why interspecific hybrids are often much better or much worse than either of the parents. We proposed that siRNAs may mediate interactions between genomes in these hybrids so that there are new patterns of gene expression that are unlike either of the parents.

sulf leaf
Paramutation in tomato. The yellow sector illustrates the effect of epigenetic silencing of the sulf locus by paramutation
To test this hypothesis we are following hybrids of cultivated and wild tomato species through to the F4 generation and have evidence that is supportive of the hypothesis (Shivaprasad et al, 2012b).

The inheritance pattern of some epigenetic changes in these hybrid plants did not always follow Mendelian ratios and, in some instances, there was evidence of a "gene drive" in which an epigenetic silenced state is transferred from one allele to another. This process resembles paramutation that has been characterised previously in maize (Gouil & Baulcombe, 2018, 2016).

We can also explore the interaction between genomes in chimaeric grafts rather than by sexual crossing because siRNA can move across a graft union and direct epigenetic change in the recipient tissue. Our initial characterisation of this mobile siRNA was in Arabidopsis (Lewsey et al, 2016; Molnar et al, 2010; Melnyk et al, 2011) and we are now testing the system in tomato.

grafted
Two tomato species grafted together

Research methodology

bioinformatic analysis
Bioinformatic analysis of tomato hybrids showing that most gene expression is in the chromosome arms rather than in the pericentromeric zone

benth
N. benthamiana
We rely heavily on next generation sequencing and, consequently, on bioinformatics (include link to bioinformatics page from current website). Gene editing has allowed us to introduce mutations into genes of interest in tomato and we also use virus-induced gene silencing. We are exploring the use of virus and other vectors to introduce the guide RNA in gene editing in N. benthamiana.

Impact

Our research can be used to explain the concepts of epigenetics, regulation and disease resistance in plants. At a practical level we aim to develop improved strategies in crop plant breeding and broad spectrum disease resistance in crops. We are also exploring the potential of epigenetically modified crops.

David Baulcombe is leading a crop science initiative with NIAB and other colleagues in the University. This Cambridge Centre for Crop Science (3CS) will facilitate collaboration in translation of research by University researchers and also by the Russell R. Geiger Professor of Crop Science for which applications are invited.

punting2018
On a picnic with the Henderson and Eves-van den Akker groups – our lab mates

References

  • Canto-Pastor A, Santos B, Valli A, Summers W, Schornack S & Baulcombe D (2019) Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato. PNAS: 396564 Available at: www.pnas.org/cgi/doi/10.1073/pnas.1814380116
  • Farnham G & Baulcombe D (2006) Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. Proc. Natl. Acad. Sci. U.S.A. 103: 18828–18833
  • Gouil Q & Baulcombe DC (2016) SLTAB2 is the paramutated SULFUREA locus in tomato. J Exp Bot 67: 2655–2664
  • Gouil Q & Baulcombe DC (2018) Paramutation-like features of natural epialleles in tomato. BMC Genomics 19: doi.org/10.1186/s12864-018-4590-4
  • Harris CJ, Slootweg EJ, Goverse A & Baulcombe DC (2013) Stepwise artificial evolution of a plant disease resistance gene. Proc. Natl. Acad. Sci. U. S. A. 110: 21189–94
  • Herr AJ, Jensen MB, Dalmay T & Baulcombe DC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science. 308: 118–120
  • Lewsey MG, Hardcastle TJ, Melnyk CW, Molnar A, Valli A, Urich MA, Nery JR, Baulcombe DC & Ecker JR (2016) Mobile small RNAs regulate genome-wide DNA methylation. Proc. Natl. Acad. Sci. U. S. A. 113: E801-810
  • Melnyk CW, Molnar A, Bassett A & Baulcombe DC (2011) Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr. Biol. 21: 1678–1683
  • Moffett P, Farnham G, Peart JR & Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 21: 4511–4519
  • Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R & Baulcombe DC (2010) Small Silencing RNAs in Plants Are Mobile and Direct Epigenetic Modification in Recipient Cells. Science. 328: 872–875
  • Peart J, Mestre P, Lu R, Malcuit I & Baulcombe D (2005) NRG1, a CC-NB-LLR protein mediates resistance against tobacco mosaic virus together with N, a TIR-NB-LRR protein. Curr. Biol. 15: 968–973
  • Shivaprasad P V., Chen H-M, Patel K, Bond DM, Santos BACM & Baulcombe DC (2012a) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24: 859–74
  • Shivaprasad P V, Dunn RM, Santos BACM, Bassett A & Baulcombe DC (2012b) Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 31: 257–66