R-loops: emerging key regulators in plants

Abstract

The biological implications of R-loops are increasingly receiving attention in plant biology. Compared with recent progresses in humans, the studies of R-loops in plants are lagging behind. Massive efforts must be invested by the plant community to better harness the possible regulatory functions of R-loops. Pioneering studies indicate that R-loops might act as key regulators of plant growth and development, and stress responses. This review thus timely updates the biological implications of R-loops and proposes a series of future lines of investigations to further decipher R-loop biology in plants. The following four aspects are included: we discuss here about the interplay between R-loops and epigenetic modifications at DNA, RNA and chromatin levels; about their regulatory roles in genome integrity, centromere functions and DNA replication; and about how they likely control plant growth and development as well as stress responses and RNA processing. Altogether, the wealth of information provided here portrays R-loop biology in plants accurately, and makes these new regulators interesting genetic levers to actuate in the aim of providing plants with new and beneficial agronomical traits.

The Influence of Edaphic Factors on DNA Damage and Repair in Wild Wheat Triticum dicoccoides Körn. (Poaceae, Triticeae)

“…Our data evidence that R-loop formation on condensed chromosomes in the M-phase ( Figure 5 ) is another potential source of chromosomal aberrations and genome instability. Generation of R-loops at transcriptionally active sites is a naturally occurring process in eukaryotic cells, including plants [ 14 , 15 , 17 , 57 ]. R-loops play an important role in gene expression, replication, and chromatin structure, whereas accumulation of aberrant R-loops causes DNA damage, particularly DSBs; in turn, DNA damage can initiate R-loop formation [ 14 , 58 , 59 ].…”

“…During transcription, the nascent RNA binds the template DNA strand, generating an RNA-DNA hybrid structure that displaces the non-template ssDNA. This three-stranded nucleic acid assembly is known as the R-loop in bacteria and eukaryotes, including plants [ 14 , 15 , 16 , 17 ]. R-loops are tightly associated with numerous cellular processes, including regulation of gene expression, replication, telomere stability, and DNA repair.…”

A ribose world: current status and future challenges of plant RNA biology

“…R-loops represent DNA–RNA structures where RNA invades the DNA double-strand ( Zheng et al ., 2023 ). R-loops associated with RDPs tend to be near transcription start sites (TSSs) and DNA regions where transcription terminates ( de Felippes and Waterhouse, 2023 ).…”

High- or Low-Yielding F2 Progeny of Wheat Is Result of Specific TaCKX Gene Coexpression Patterns in Association with Grain Yield in Paternal Parent

“…Such nonadditive gene expression levels associated with phenotypic heterosis in F 1 plants have already been reported and reviewed [ 29 , 30 , 31 , 32 , 33 ]. These deviations from the general role are the result of different factors, such as epigenetic regulation by transcription factors [ 34 , 35 , 36 , 37 , 38 ], the balance of gene dosage [ 39 , 40 ], small interfering RNAs (sRNA) [ 36 , 41 ], histone modifications [ 42 ], R-loop formation [ 43 ], or distally acting factors [ 31 ]. Furthermore, noncoding RNAs have been described as regulators of the development of shoots and grains in barley [ 44 ] and dominant epigenetic regulators of early meiotic stages in wheat, ensuring reproductive success [ 45 ].…”