Transgenerational Paternal Inheritance of TaCKX GFMs Expression Patterns Indicate a Way to Select Wheat Lines with Better Parameters for Yield-Related Traits

Abstract

Members of the TaCKX gene family (GFMs) encode the cytokinin oxygenase/dehydrogenase enzyme (CKX), which irreversibly degrades cytokinins in the organs of wheat plants; therefore, these genes perform a key role in the regulation of yield-related traits. The purpose of the investigation was to determine how expression patterns of these genes, together with the transcription factor-encoding gene TaNAC2-5A, and yield-related traits are inherited to apply this knowledge to speed up breeding processes. The traits were tested in 7 days after pollination (DAP) spikes and seedling roots of maternal and paternal parents and their F2 progeny. The expression levels of most of them and the yield were inherited in F2 from the paternal parent. Some pairs or groups of genes cooperated, and some showed opposite functions. Models of up- or down-regulation of TaCKX GFMs and TaNAC2-5A in low-yielding maternal plants crossed with higher-yielding paternal plants and their high-yielding F2 progeny reproduced gene expression and yield of the paternal parent. The correlation coefficients between TaCKX GFMs, TaNAC2-5A, and yield-related traits in high-yielding F2 progeny indicated which of these genes were specifically correlated with individual yield-related traits. The most common was expressed in 7 DAP spikes TaCKX2.1, which positively correlated with grain number, grain yield, spike number, and spike length, and seedling root mass. The expression levels of TaCKX1 or TaNAC2-5A in the seedling roots were negatively correlated with these traits. In contrast, the thousand grain weight (TGW) was negatively regulated by TaCKX2.2.2, TaCKX2.1, and TaCKX10 in 7 DAP spikes but positively correlated with TaCKX10 and TaNAC2-5A in seedling roots. Transmission of TaCKX GFMs and TaNAC2-5A expression patterns and yield-related traits from parents to the F2 generation indicate their paternal imprinting. These newly shown data of nonmendelian epigenetic inheritance shed new light on crossing strategies to obtain a high-yielding F2 generation.

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

“…As presented in this research, grain yield was inherited in F 2 progeny as in the pater, regardless of awned or awnless spike cultivars. The same was documented in our previous research with awnless wheat cultivars [ 24 ]. It is difficult to indicate the common pattern of coexpression of TaCKX genes, which should be represented in the high-yielding pater to transmit this pattern of expression together with the yield to F 2 generation.…”

“…In our previous research [ 24 ], it was documented for the first time that the expression levels of most of the yield-related TaCKX genes, TaNAC2-5A , and grain yield were inherited in F 2 from the paternal parent. The experiment was carried out using reciprocal crosses of awnless cultivars.…”

“…In the silencing experiment, the down-regulation of wheat TaCKX1 resulted in a strong down-regulation of TaCKX1 and 11 and up-regulation of TaCKX2.1 and others in both awnless and awned cultivars; however, it affected different yield-related traits, and only in the awned one, it resulted in a high-yielding phenotype [ 20 , 22 ]. Similarly, the spike TaCKX2.1 , which is positively correlated with grain number, grain yield, spike number, spike length, and root mass, was coupled with other TaCKX GFMs, and in the case of grain yield, it was negatively correlated with the spike and root TaCKX1 in the high-yielding F 2 progeny [ 24 ]. In addition to this specific coregulation, TaCKX1 , 2.1 , and 5 could be regulated by JUNGBRUNNEN 1-like TF, renamed TaNACJ-1 and TaNAC94 TF [ 25 ].…”

“…Since the TaCKX gene expression pattern is related to wheat yield parameters, it was interesting to check how this pattern is inherited. In our earlier research with TaCKX GFMs, we also included TaNAC2-5A , which encodes the NAC-type transcription factor [ 22 , 23 , 24 , 25 ]. The TaNAC2-5A was found to increase wheat yield by controlling the nitrate response [ 26 , 27 ], and in our research, the gene was coexpressed with selected TaCKX GFMs and was correlated with several yield-related traits.…”

“…Since crossbreeding and selection are the basic steps in breeding, and the expression pattern of TaCKX genes regulates yield-related traits, it was important to check how the expression patterns of these genes together with yield-related traits are inherited. In our primary report on the transgenerational inheritance of agronomically important genes, we tested the expression patterns of TaCKX genes and TaNAC2-5A in segregating the F 2 generation of reciprocal crosses of polyploid wheat [ 24 ]. We documented that some of them were paternally imprinted, together with the yield parameter.…”