Abstract
Low-phosphorus (P) stress is one of the major factors constraining plant growth and yield. Improving plant tolerance to P starvation through molecular breeding is an efficient alternative to increase grain production. In the study, 331 diverse maize inbreds were used to detect nucleotide diversity and favorable alleles of ZmARF31, which plays a key role in low P responses and root architecture regulation. Significant phenotypic variation was found in each of 11 tested traits under both P and no-P treatments, and 30 single nucleotide polymorphisms (SNPs) and 14 insertion–deletions (InDels) were detected in ZmARF31 among the 331 maize inbreds. The 5′-untranslated region (UTR) of ZmARF31 showed a small linkage disequilibrium (LD) block under significant purifying selection, whereas the 3′-UTR showed the most abundant diversity and a larger LD block. Thirty, fourteen, and nine natural variations were identified in ZmARF31 that were associated with P-deficiency-tolerance traits (P ≤ 0.01) by using the general linear model (GLM), GLM incorporated with population structure, and mixed linear model, respectively. Four SNPs were significantly associated with the total dry weight (TDW) in the three models, of which SNPs S410 and S462 were located in a complete LD block. A further verification conducted in a recombinant inbred line population revealed that favorable allele G/G of non-synonymous mutation S410 and favorable allele with a 38 bp insertion of InDel S1442 exhibited positive genetic effects on the TDW and total root tips, respectively. Expression analysis further confirmed that ZmARF31 was highly expressed in the roots of low-P-tolerant inbred 178. The protein encoded by ZmARF31 was located both in the nucleus and cytoplasm. Haplotypes carrying more favorable alleles showed a greater effect on phenotypic variation than single loci. Such haplotypes should be helpful to develop valuable genetic markers and perform maize molecular breeding.
Highlights
In plants, phosphorus (P) is a critical macronutrient and plays an important role in various basic biological functions such as energy generation, glycolysis, nucleic acid synthesis, enzyme activation/inactivation, redox reactions, signaling, and carbon metabolism (Rausch and Bucher, 2002; Cordell et al, 2009; Shen et al, 2011)
All the traits were significantly influenced by P starvation, which could be used for further genetic analysis
The natural variation within ZmARF31 gene was detected by determining the levels of nucleotide diversity in ZmARF31 by using 331 maize lines and eight teosinte lines
Summary
Phosphorus (P) is a critical macronutrient and plays an important role in various basic biological functions such as energy generation, glycolysis, nucleic acid synthesis, enzyme activation/inactivation, redox reactions, signaling, and carbon metabolism (Rausch and Bucher, 2002; Cordell et al, 2009; Shen et al, 2011). The auxin response factor (ARF), one of the transcription factors (TFs), plays a key role in low P responses and phenotypic variation by altering gene expression and function (CalderonVazquez et al, 2011). In Arabidopsis, ARFs involved in the regulation of root architecture are the most important regulators of downstream starvationinduced genes (Okushima et al, 2005, 2007; Gutierrez et al, 2009). Target-gene analysis of arf7–arf transgenic plants revealed that ARFs regulated lateral root formation via the direct activation of lateral organ boundaries domain/asymmetric leaves (LBD/ASLs) in Arabidopsis (Okushima et al, 2007). The conserved domains of ZmARF31 in maize are highly similar to those of AtARF19 in Arabidopsis, with known function in root growth and development (Okushima et al, 2007)
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