Non-canonical regulation of SPL transcription factors by a human OTUB1-like deubiquitinase defines a new plant type rice associated with higher grain yield

Abstract

Achieving increased grain productivity has long been the overriding focus of cereal breeding programs. The ideotype approach has been used to improve rice yield potential at the International Rice Research Institute and in China. However, the genetic basis of yield-related traits in rice remains unclear. Here, we show that a major quantitative trait locus, qNPT1, acts through the determination of a 'new plant type' (NPT) architecture characterized by fewer tillers, sturdier culms and larger panicles, and it encodes a deubiquitinating enzyme with homology to human OTUB1. Downregulation of OsOTUB1 enhances meristematic activity, resulting in reduced tiller number, increased grain number, enhanced grain weight and a consequent increase in grain yield in rice. Unlike human OTUB1, OsOTUB1 can cleave both K48- and K63-linked polyubiquitin. OsOTUB1 interacts with the E2 ubiquitin-conjugating protein OsUBC13 and the squamosa promoter-binding protein-like transcription factor OsSPL14. OsOTUB1 and OsSPL14 share common target genes, and their physical interaction limits K63-linked ubiquitination (K63Ub) of OsSPL14, which in turn promotes K48Ub-dependent proteasomal degradation of OsSPL14. Conversely, loss-of-function of OsOTUB1 is correlated with the accumulation of high levels of OsSPL14, resulting in the NPT architecture. We also demonstrated that pyramiding of high-yielding npt1 and dep1-1 alleles provides a new strategy for increasing rice yield potential above what is currently achievable.

Variation in the regulatory region of FZP causes increases in secondary inflorescence branching and grain yield in rice domestication

“…We propose that an alternative approach is the post‐transcriptional protein turnover of FZP mediated by NAL1. In rice, a similar approach was also found in the manipulation of IDEAL PLANT ARCHITECTURE 1 (IPA1), in which ubiquitination or deubiquitination of IPA1 mediated by IPA1 INTERACTING PROTEIN 1 (IPI1) or OsOTUB1 could precisely balance the endogenous IPA1 levels to modulate rice plant architecture and grain yields (Wang et al ., ,b), suggesting that post‐transcriptional manipulation of protein turnover plays an important role in controlling inflorescence branching. Indeed, upregulating NAL1 expression can slightly reduce FZP accumulation in the inflorescence, and thus enhance rice grain yield.…”

Overexpression of OsSPL14 results in transcriptome and physiology changes in indica rice ‘MH86’

“…A RING-finger E3 ligase, IPA1 INTERACTING PROTEIN1 (IPI1), could regulate the protein levels of IPA1/OsSPL14 in different tissues (Wang et al 2017a). A human ovarian tumor domaincontaining ubiquitin aldehyde-binding protein 1 like deubiquitinating enzyme in rice could promote the degradation of IPA1/OsSPL14 indirectly (Wang et al 2017b). DWARF 53 (D53), a key repressor of the strigolactone (SL) signaling pathway, suppresses the transcription of IPA1/OsSPL14 (Song et al 2017).…”

New path towards a better rice architecture

“…To explore this possibility, the IPI1 discussed here could be a good candidate as it does not appear to sacrifice tiller number for increased grains per panicle. Furthermore, the paper about OsOTUB1 by Wang et al [4], alongside with the paper about IPI1 [10], strongly suggests that the mode of ubiquitination of IPA1/OsSPL14 (K48-or K63-linked) regulates its stability in an organ-specific manner and consequently controls the NPT or ideal rice architecture, although the detailed molecular mechanism for this has not yet been fully clarified.…”

“…Indeed, most genes inducing large panicle, such as IPA1/OsSPL14 [4] and SCM3/OsTB1 [11], can increase the grain number per panicle, but at the same time, decrease the tiller number per plant. In the same manner, the OsOTUB1 discussed by Wang et al also appears to follow the same trade-off trend, but with good results in terms of high grain yield and lodging resistance.…”

“…In a recent paper in Cell Research, Wang et al [4] report a gene involved in the NPT architecture. The gene was identified through QTL analysis and positional cloning using japonica-indica crosses and was named as rice OTUB1 (OsOTUB1) because of its homology to human OTUB1 (ovarian tumor domain-containing ubiquitin aldehydebinding protein 1).…”