In:
Science, American Association for the Advancement of Science (AAAS), Vol. 377, No. 6604 ( 2022-07-22)
Abstract:
Rapid population growth, rising meat consumption, and the expanding use of crops for nonfood and nonfeed purposes increase the pressure on global food production. At the same time, the excessive use of nitrogen fertilizer to enhance agricultural production poses serious threats to both human health and the environment. To achieve the required yield increases and make agriculture more sustainable, intensified breeding and genetic engineering efforts are needed to obtain new crop varieties with higher photosynthetic capacity and improved nitrogen use efficiency (NUE). However, progress has been slow, largely due to the limited knowledge about regulator genes that potentially can coordinately optimize carbon assimilation and nitrogen utilization. RATIONALE Transcription factors control diverse biological processes by binding to the promoters (or intragenic regions) of target genes, and a number of transcription factors have been identified that control carbon fixation and nitrogen assimilation. A previous comparative analysis of maize and rice leaf transcriptomes and metabolomes revealed a set of 118 candidate transcription factors that may act as regulators of C 4 photosynthesis. We screened these transcription factors for their responsiveness to light and nitrogen supply in rice, and found that the gene Dehydration-Responsive Element-Binding Protein 1C ( OsDREB1C ), a member of the APETALA2/ethylene-responsive element binding factor (AP2/ERF) family, exhibits properties expected of a regulator that can simultaneously modulate photosynthesis and nitrogen utilization. RESULTS OsDREB1C expression is induced in rice by both light and low-nitrogen status. We generated overexpression lines ( OsDREB1C -OE) and knockout mutants ( OsDREB1C -KO) in rice, and conducted field trials in northern, southeastern, and southern China from 2018 to 2021. OsDREB1C -OE plants exhibited 41.3 to 68.3% higher yield than wild-type (WT) plants due to increased grain number per panicle, elevated grain weight, and enhanced harvest index. We observed that light-induced growth promotion of OsDREB1C -OE plants was accompanied by enhanced photosynthetic capacity and concomitant increases in photosynthetic assimilates. In addition, 15 N feeding experiments and field studies with different nitrogen fertilization regimes revealed that NUE was improved in OsDREB1C- OE plants due to elevated nitrogen uptake and transport activity. Moreover, OsDREB1C overexpression led to more efficient carbon and nitrogen allocation from source to sink, thus boosting grain yield, particularly under low-nitrogen conditions. Additionally, the OsDREB1C -OE plants flowered 13 to 19 days earlier and accumulated higher biomass at the heading stage than WT plants under long-day conditions. OsDREB1C is localized in the nucleus and the cytosol and functions as a transcriptional activator that directly binds to cis elements in the DNA, including dehydration-responsive element (DRE)/C repeat (CRT), GCC, and G boxes. Chromatin immunoprecipitation sequencing (ChIP-seq) and transcriptomic analyses identified a total of 9735 putative OsDREB1C-binding sites at the genome-wide level. We discovered that five genes targeted by OsDREB1C [ ribulose-l,5-bisphosphate carboxylase/oxygenase small subunit 3 ( OsRBCS3 ), nitrate reductase 2 ( OsNR2 ), nitrate transporter 2.4 ( OsNRT2.4 ), nitrate transporter 1.1B ( OsNRT1.1B ), and flowering locus T-like 1 ( OsFTL1 )] are closely associated with photosynthesis, nitrogen utilization, and flowering, the key traits altered by OsDREB1C overexpression. ChIP-quantitative polymerase chain reaction (ChIP-qPCR) and DNA affinity purification sequencing (DAP-seq) assays confirmed that OsDREB1C activates the transcription of these genes by binding to the promoter of OsRBCS3 and to exons of OsNR2 , OsNRT2.4 , OsNRT1.1B , and OsFTL1 . By showing that biomass and yield increases can also be achieved by OsDREB1C overexpression in wheat and Arabidopsis , we have demonstrated that the mode of action and the biological function of the transcription factor are evolutionarily conserved. CONCLUSION Overexpression of OsDREB1C not only boosts grain yields but also confers higher NUE and early flowering. Our work demonstrates that by genetically modulating the expression of a single transcriptional regulator gene, substantial yield increases can be achieved while the growth duration of the crop is shortened. The existing natural allelic variation in OsDREB1C , the highly conserved function of the transcription factor in seed plants, and the ease with which its expression can be altered by genetic engineering suggest that this gene could be the target of future crop improvement strategies toward more efficient and more sustainable food production. OsDREB1C coordinates yield and growth duration. OsDREB1C was identified by its responsiveness to light and low nitrogen in a screen of 118 transcription factors related to C 4 photosynthesis. Transcriptional activation of multiple downstream target genes by OsDREB1C confers enhanced photosynthesis, improved nitrogen utilization, and early flowering. Together, the activated genes cause substantial yield increases in rice and wheat.
Type of Medium:
Online Resource
ISSN:
0036-8075
,
1095-9203
DOI:
10.1126/science.abi8455
Language:
English
Publisher:
American Association for the Advancement of Science (AAAS)
Publication Date:
2022
detail.hit.zdb_id:
128410-1
detail.hit.zdb_id:
2066996-3
detail.hit.zdb_id:
2060783-0
SSG:
11
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