Impact of Agrobacterium tumefaciens-induced stem tumors on NO 3 − uptake in Ricinus communis

Abstract

Developing tumors induced by Agrobacterium tumefaciens, strain C58, on stems of Ricinus communis L. var. gibsonii cv. Carmencita were shown to be strong metabolic sinks for sucrose and amino acids, thus causing higher nutrient demand in the host plant. However, NO 3 − uptake and, to a lesser extent, also H2PO 4 − uptake were strongly inhibited. Correspondingly, NO 3 − concentration was lower in tumorised than in the control plants. NO 3 − reductase activity was the same in both plant types, but it was completely suppressed in the tumors. The electrical membrane potential difference of root cells was unaffected in tumorised plants when soil-grown, but significantly lowered when grown hydroponically. Consistent with the low NO 3 − uptake rate, NO 3 − -dependent membrane depolarisation at the onset of NO 3 − /2H+-cotransport was nearly zero. In the phloem sap, sucrose and amino acid concentrations were considerably lower in tumorised than in control plants, and lower below than above the tumor. The qualitative pattern of amino acids of the phloem sap of stems was almost the same in tumorised and control plants. It is concluded that neither the overall amino acid concentration nor special amino acids nor ammonium in the transport phloem suppress NO 3 − uptake in the roots. Aminocyclopropane-carboxylate, the precursor of ethylene, which is produced in the tumors in high amounts, was low in the stems and the same in both plant types. Thus, ACC and ethylene were ruled out as directly interfering with nutrient uptake in the roots. Root morphology was strongly affected during tumor development. Root fresh weight decreased to 50% of the controls and lateral root development was almost completely prevented. This suggests that the high tumor ethylene production, together with an increasing concentration of phenolic compounds, severely inhibits the basipetal auxin flow to the roots. Auxin accumulation and retention was confirmed by specifically enhanced expression of the auxin-responsive promoter of the soybean gene GH3:GUS in tumors induced in transgenic Trifolium repens L. Hence, root development is poorer and anion uptake inhibited in tumorised plants. This may be aggravated by abscisic acid accumulation in the tumor and its basipetal export into the roots. Moreover, sucrose depletion of the sieve tubes leads to energy shortage at the root level for maintaining energy-dependent anion uptake.