Genome-Wide Identification of Sultr Genes in Malus domestica and Low Sulfur-Induced MhSultr3;1a to Increase Cysteine-Improving Growth

Abstract

Sulfur is an essential nutrient for plant growth and development. Sulfate transporters (Sultrs) are critical for sulfate ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="M1"><mml:msubsup><mml:mrow><mml:mtext>SO</mml:mtext></mml:mrow><mml:mrow><mml:mn>4</mml:mn></mml:mrow><mml:mrow><mml:mn>2</mml:mn><mml:mo>-</mml:mo></mml:mrow></mml:msubsup></mml:math> ) uptake from the soil by the roots in higher plants. However, knowledge about Sultrs in apples ( Malus domestica ) is scarce. Here, nine putative MdSultrs were identified and classified into two groups according to the their phylogenetic relationships, gene structures, and conserved motifs. Various cis-regulatory elements related to abiotic stress and plant hormone responsiveness were found in the promoter regions of MdSultrs . These MdSultrs exhibited tissue-specific expression patterns and responded to low sulfur (S), abscisic acid (ABA), indole-3-acetic acid (IAA), and methyl jasmonate (MeJA), wherein MdSultr3;1a was especially expressed in the roots and induced by low S. The uptake of <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="M2"><mml:msubsup><mml:mrow><mml:mtext>SO</mml:mtext></mml:mrow><mml:mrow><mml:mn>4</mml:mn></mml:mrow><mml:mrow><mml:mn>2</mml:mn><mml:mo>-</mml:mo></mml:mrow></mml:msubsup></mml:math> in cultivated apples depends on the roots of its rootstock, and MhSultr3;1a was isolated from Malus hupehensis roots used as a rootstock. MhSultr3 ;1a shared 99.85% homology with MdSultr3;1a and localized on the plasma membrane and nucleus membrane. Further function characterization revealed that MhSultr3;1a complemented an <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="M3"><mml:msubsup><mml:mrow><mml:mtext>SO</mml:mtext></mml:mrow><mml:mrow><mml:mn>4</mml:mn></mml:mrow><mml:mrow><mml:mn>2</mml:mn><mml:mo>-</mml:mo></mml:mrow></mml:msubsup></mml:math> transport-deficient yeast mutant and improved the growth of yeast and apple calli under low S conditions. The MhSultr3;1a -overexpressing apple calli had a higher fresh weight compared with the wild type (WT) under a low-S treatment because of the increased <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="M4"><mml:msubsup><mml:mrow><mml:mtext>SO</mml:mtext></mml:mrow><mml:mrow><mml:mn>4</mml:mn></mml:mrow><mml:mrow><mml:mn>2</mml:mn><mml:mo>-</mml:mo></mml:mrow></mml:msubsup></mml:math> and cysteine (Cys) content. These results demonstrate that MhSultr3;1a may increase the content of <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="M5"><mml:msubsup><mml:mrow><mml:mtext>SO</mml:mtext></mml:mrow><mml:mrow><mml:mn>4</mml:mn></mml:mrow><mml:mrow><mml:mn>2</mml:mn><mml:mo>-</mml:mo></mml:mrow></mml:msubsup></mml:math> and Cys to meet the demands of S-containing compounds and improve their growth under S-limiting conditions.