Wheat plant height locus RHT25 encodes a PLATZ transcription factor that interacts with DELLA (RHT1)

Plant height is an important agronomic trait with a significant impact on grain yield, as demonstrated by the positive effect of the REDUCED HEIGHT (RHT) dwarfing alleles (Rht1b) on lodging and harvest index in the “Green Revolution” wheat varieties. However, these gibberellic acid (GA) insensitive alleles also reduce coleoptile length, biomass production, and yield potential in some environments, triggering the search for alternative GA-sensitive dwarfing genes. Here we report the identification, validation and characterization of the gene underlying the GA-sensitive dwarfing locus RHT25 in wheat. This gene, designated as PLATZ-A1 (TraesCS6A02G156600), is expressed mainly in the elongating stem and developing spike and encodes a plant-specific AT-rich sequence- and zinc-binding protein (PLATZ). Natural and induced loss-of-function mutations in PLATZ-A1 reduce plant height and its over-expression increases it, demonstrating that PLATZ-A1 is the causative gene of RHT25. PLATZ-A1 interacts physically and genetically with RHT1 (DELLA), and both genes have stronger effects on plant height in the presence of the wildtype than in the presence of the mutant allele of the other gene. These results suggest that PLATZ1 can modulate the effect of DELLA on wheat plant height. We identified four natural truncation mutations and one promoter insertion in PLATZ-A1 that are more frequent in modern varieties than in landraces, suggesting positive selection during wheat breeding. These mutations can be used to fine-tune wheat plant height and, in combination with other GA-sensitive dwarfing genes, to replace the GA-insensitive Rht1b alleles to search for grain yield improvements beyond those of the Green Revolution varieties. Significance Statement We have identified and characterized a previously unknown gene controlling plant height in wheat and named it PLATZ1. Mutations in PLATZ1 reduce plant height while its overexpression results in taller plants. PLATZ1 is expressed mainly in elongating stems and developing spikes and interacts physically and genetically with the “Green Revolution” dwarfing gene REDUCED HEIGHT 1 (RHT1). We discovered five natural mutants in the A genome copy of PLATZ1 in common wheat that have been favored during breeding, suggesting an overall positive effect on wheat performance. These mutations can be used to fine-tune wheat plant height and, eventually, to replace the RHT1 dwarfing alleles that impose limitations on planting depth and grain yield potential in some environments.

[1]  Mingming Xin,et al.  Histone acetyltransferase TaHAG1 interacts with TaPLATZ5 to activate TaPAD4 expression and positively contributes to powdery mildew resistance in wheat , 2022, The New phytologist.

[2]  J. Dubcovsky,et al.  Transcriptional signatures of wheat inflorescence development , 2022, bioRxiv.

[3]  S. Walkowiak,et al.  An autoactive NB-LRR gene causes Rht13 dwarfism in wheat , 2022, bioRxiv.

[4]  B. Carver,et al.  TaCol-B5 modifies spike architecture and enhances grain yield in wheat , 2022, Science.

[5]  Xuewei Chen,et al.  The PGS1 basic helix‐loop‐helix protein regulates Fl3 to impact seed growth and grain yield in cereals , 2022, Plant biotechnology journal.

[6]  Mingming Xin,et al.  A natural variation in Ribonuclease H-like gene underlies Rht8 to confer "Green Revolution" trait in wheat. , 2022, Molecular plant.

[7]  Muhammad Adeel Hassan,et al.  Rht24b, an ancient variation of TaGA2ox-A9, reduces plant height without yield penalty in wheat. , 2021, The New phytologist.

[8]  G. Brown-Guedira,et al.  Identification and characterization of a natural polymorphism in FT-A2 associated with increased number of grains per spike in wheat , 2021, TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik.

[9]  J. Dubcovsky,et al.  WAPO-A1 is the causal gene of the 7AL QTL for spikelet number per spike in wheat , 2021, bioRxiv.

[10]  D. Van Der Straeten,et al.  N-Terminal Truncated RHT-1 Proteins Generated by Translational Reinitiation Cause Semi-Dwarfing of Wheat Green Revolution Alleles. , 2021, Molecular plant.

[11]  Mengping Cheng,et al.  Identification and Characterization of PLATZ Transcription Factors in Wheat , 2022 .

[12]  Bernardo J. Clavijo,et al.  Multiple wheat genomes reveal global variation in modern breeding , 2020, Nature.

[13]  P. Langridge,et al.  Green revolution "stumbles" in a dry environment: Dwarf wheat with Rht genes fails to produce higher grain yield than taller plants under drought. , 2020, Plant, cell & environment.

[14]  H. Xue,et al.  The rice PLATZ protein SHORT GRAIN6 determines grain size by regulating spikelet hull cell division. , 2020, Journal of integrative plant biology.

[15]  Xuehui Huang,et al.  The PLATZ Transcription Factor GL6 Affects Grain Length and Number in Rice. , 2019, Plant physiology.

[16]  Jinfang Chu,et al.  A wheat dominant dwarfing line with Rht12, which reduces stem cell length and affects gibberellic acid synthesis, is a 5AL terminal deletion line , 2019, The Plant journal : for cell and molecular biology.

[17]  K. Jordan,et al.  Registration of the Triticeae‐CAP Spring Wheat Nested Association Mapping Population , 2019, Journal of Plant Registrations.

[18]  Jonathan D. G. Jones,et al.  Shifting the limits in wheat research and breeding using a fully annotated reference genome , 2018, Science.

[19]  Kun Wu,et al.  Modulating plant growth-metabolism coordination for sustainable agriculture , 2018, Nature.

[20]  J. Dubcovsky,et al.  Identification and characterization of Rht25, a locus on chromosome arm 6AS affecting wheat plant height, heading time, and spike development , 2018, Theoretical and Applied Genetics.

[21]  H. Nam,et al.  ORESARA15, a PLATZ transcription factor, mediates leaf growth and senescence in Arabidopsis. , 2018, The New phytologist.

[22]  A. Carter,et al.  Identification and validation of QTL for grain yield and plant water status under contrasting water treatments in fall-sown spring wheats , 2018, Theoretical and Applied Genetics.

[23]  B. Steuernagel,et al.  Rht18 Semidwarfism in Wheat Is Due to Increased GA 2-oxidaseA9 Expression and Reduced GA Content1[OPEN] , 2018, Plant Physiology.

[24]  Leah Clissold,et al.  Uncovering hidden variation in polyploid wheat , 2017, Proceedings of the National Academy of Sciences.

[25]  Cristobal Uauy,et al.  A splice acceptor site mutation in TaGW2-A1 increases thousand grain weight in tetraploid and hexaploid wheat through wider and longer grains , 2016, Theoretical and Applied Genetics.

[26]  Hadi Quesneville,et al.  Structural and functional partitioning of bread wheat chromosome 3B , 2014, Science.

[27]  John M. Martin,et al.  Genetic Basis of Agronomic Differences between a Modern and a Historical Spring Wheat Cultivar , 2014 .

[28]  M. Gooding,et al.  Gibberellin-responsive and -insensitive dwarfing alleles on wheat performance in contrasting tillage systems , 2013 .

[29]  C. Steber,et al.  Gibberellin Signaling: A Theme and Variations on DELLA Repression1 , 2012, Plant Physiology.

[30]  M. Gooding,et al.  Effect of wheat dwarfing genes on nitrogen-use efficiency , 2011, The Journal of Agricultural Science.

[31]  Masatomo Kobayashi,et al.  Accumulation of Phosphorylated Repressor for Gibberellin Signaling in an F-box Mutant , 2003, Science.

[32]  H. Furuhashi,et al.  A novel class of plant-specific zinc-dependent DNA-binding protein that binds to A/T-rich DNA sequences. , 2001, Nucleic acids research.

[33]  P. Christou,et al.  ‘Green revolution’ genes encode mutant gibberellin response modulators , 1999, Nature.

[34]  F. Salamini,et al.  Catalogue of gene symbols for wheat , 1998 .

[35]  A. Börner,et al.  Optimizing wheat grain yield: effects of Rht (gibberellin-insensitive) dwarfing genes , 1997, The Journal of Agricultural Science.