Transcriptome Association Identifies Regulators of Wheat Spike Architecture

Abstract

The architecture of wheat (Triticum aestivum) inflorescence and its complexity is among the most important agronomic traits that influence yield. For example, wheat spikes vary considerably in the number of spikelets, which are specialized reproductive branches, and the number of florets, which are spikelet branches that produce seeds. The large and repetitive nature of the three homologous and highly similar subgenomes of wheat has impeded attempts at using genetic approaches to uncover beneficial alleles that can be utilized for yield improvement. Using a population-associative transcriptomic approach, we analyzed the transcriptomes of developing spikes in 90 wheat lines comprising 74 landrace and 16 elite varieties and correlated expression with variations in spike complexity traits. In combination with coexpression network analysis, we inferred the identities of genes related to spike complexity. Importantly, further experimental studies identified regulatory genes whose expression is associated with and influences spike complexity. The associative transcriptomic approach utilized in this study allows rapid identification of the genetic basis of important agronomic traits in crops with complex genomes.Grains of cereal crops provide a major source of human diet and nutrition. Improving grain yield is a primary objective during crop domestication and a major goal of crop-breeding programs. Inflorescence (spike) architecture dictates the capacity for seed production in cereal crops, including wheat (Triticum aestivum), the world's most widely grown cereal. In the archetypal bread wheat spike, the inflorescence meristem forms a limited number of lateral spikelet meristems (SMs) per rachis node, and a single terminal SM at the distal end. Each SM is indeterminate and typically produces two to four fertile florets that produce seeds (Fig. 1A; Supplemental Fig. S1; Bonnett, 1936;Fisher, 1973). Like maize (Zea mays) and rice (Oryza sativa), wheat yield per plant largely depends on the number of florets per spike and thus spike architecture. The numbers of SMs (and rachises) and florets per spikelet are major target traits for efforts aimed at improving wheat yield. In addition, the number of SMs per rachis may be increased to increase floret number, as in rare supernumerary spikelet variations.In rice, maize, and barley (Hordeum vulgare), multiple genes regulating spike development have been identified (Sreenivasulu and Schnurbusch, 2012;Tanaka et al., 2013). However, our understanding of wheat spike development remains rudimentary at the molecular level. In wheat, increased transcription levels of Q, an AP2-like gene, was markedly associated with spike compactness, suggesting that the Q gene may be implicated in spike development (Simons et al., 2006), although its role in spike complexity remains unclear. Feng et al. (2017) underlying the genetic regulation of rare supernumerary spikelet variations. For example, wheat Photoperiod1 (Ppd1) was identified as a regulator of paired spikelet formation (Boden et al., 2...

Genetic pathways controlling inflorescence architecture and development in wheat and barley

“…Similar comparisons of reciprocal gene function in wheat and barley, such as Vrs1 and HOX2 , will advance our understanding of the genetic regulation of inflorescence development within each species, while also contributing to our knowledge about the biological processes that contribute to the diverse architectures of wheat and barley (Komatsuda et al ; Sakuma et al ; Wang et al ; Sakuma et al ). This investigation will be facilitated by the mutant populations generated recently for barley, tetraploid wheat and hexaploid wheat, which can be used in a forward genetics approach to identify novel inflorescence development genes, and in a reverse genetics approach to investigate the function of known inflorescence architecture genes in the respective species (Caldwell et al ; Krasileva et al ).…”

“…To complement the genetic advancement in our understanding of the genetic regulation of inflorescence architecture, recent improvements in the sequence of the barley and wheat genomes have facilitated the use of genome‐wide transcriptome analysis to identify novel regulators of inflorescence development (Digel et al ; Pearce et al ; Borrill et al ; Mascher et al ; Wang et al ; IWGSC ; Ramirez‐Gonzalez et al ). For example, in barley, analysis of multiple stages of inflorescence development identified genes important for the vegetative‐to‐reproductive transition, including the MADS box transcription factors BARLEY MADS BOX1 ( BM1 ) and VEGETATIVE TO REPRODUCTIVE TRNASITION2 ( VRT2 ) that are repressed during the transition, and genes including SQUAMOSA PROMOTER BINDING‐LIKE PROTEIN4 ( SPL4 ), KNOTTED1 ( KN1 ) and SUPPRESSOR OF CONSTANS1 ( SOC1 ) that were activated (Digel et al ).…”

“…Similar transcriptome profiling was also performed in wheat to identify genes whose expression is associated with key yield‐related traits, including spikelet and floret numbers (Wang et al ). While this analysis used a less conventional nomenclature of developmental stages, it did identify TaPAP2 (a wheat orthologue of the rice gene, PAP2 , which is more commonly referred to as AGLG1 [ AGAMOUS‐LIKE GENE1 ] in wheat), WFZP , LAX PANICLE1 ( LAX1 ) and TERMINAL FLOWER1 ( TFL1 ) as genes whose expression was associated significantly with spikelet number (Yan et al ; Zhao et al ; Boden et al ; Wang et al ).…”

“…Similar transcriptome profiling was also performed in wheat to identify genes whose expression is associated with key yield‐related traits, including spikelet and floret numbers (Wang et al ). While this analysis used a less conventional nomenclature of developmental stages, it did identify TaPAP2 (a wheat orthologue of the rice gene, PAP2 , which is more commonly referred to as AGLG1 [ AGAMOUS‐LIKE GENE1 ] in wheat), WFZP , LAX PANICLE1 ( LAX1 ) and TERMINAL FLOWER1 ( TFL1 ) as genes whose expression was associated significantly with spikelet number (Yan et al ; Zhao et al ; Boden et al ; Wang et al ). Over‐expressing PAP2/AGLG1 decreased inflorescence length, spikelet and floret numbers in a way consistent with its role as a floral activator, whereas overexpression of TFL1 facilitated development of additional spikelets and florets that supports a function for TFL1 in maintaining meristem dormancy and delaying the vegetative‐to‐reproductive transition (Wang et al ).…”

“…While this analysis used a less conventional nomenclature of developmental stages, it did identify TaPAP2 (a wheat orthologue of the rice gene, PAP2 , which is more commonly referred to as AGLG1 [ AGAMOUS‐LIKE GENE1 ] in wheat), WFZP , LAX PANICLE1 ( LAX1 ) and TERMINAL FLOWER1 ( TFL1 ) as genes whose expression was associated significantly with spikelet number (Yan et al ; Zhao et al ; Boden et al ; Wang et al ). Over‐expressing PAP2/AGLG1 decreased inflorescence length, spikelet and floret numbers in a way consistent with its role as a floral activator, whereas overexpression of TFL1 facilitated development of additional spikelets and florets that supports a function for TFL1 in maintaining meristem dormancy and delaying the vegetative‐to‐reproductive transition (Wang et al ). Interestingly, Wang and colleagues also overexpressed a homologue of HvHOX2 , which reduced spikelet and floret numbers and inflorescence length to indicate a possible divergence in function relative to barley (Sakuma et al ; Sakuma et al ; Wang et al ).…”