Drought stress-induced irregularities in male organ development cause stage-specific morpho-physiological and transcriptome changes in tomato

Drought limits the growth and productivity of plants. Reproductive development is sensitive to drought but the underlying physiological and molecular mechanisms remain unclear in tomato. Here, we investigated drought effect on tomato floral development using morpho-physiological and transcriptome analyses. Drought induced bud and flower abortions, and reduced fruit set/yield, triggered by male sterility due to abnormal anther and pollen development. Under drought stress (DS), anthers at pollen mother cell to meiotic (PMC-MEI) stage survived while anthers at tetrad to uninucleate microspore (TED-VUM) stage aborted. PMC-MEI stage had lower ABA increase, reduced IAA and higher sugar contents under DS relative to well-watered. However, TED-VUM stage had higher ABA increase, higher IAA level and no accumulation of soluble sugars, indicating abnormal carbohydrate and hormone metabolisms. Moreover, RNA-Seq analysis identified altogether ˃15,000 differentially expressed genes that were assigned to multiple pathways, suggesting tomato anthers utilize complicated mechanisms to cope with drought. Major genes involved in tapetum/microspore development and ABA homeostasis were drought-induced while those involved in sugar utilization and IAA metabolism were repressed at PMC-MEI stage. Our results suggest crosstalks between phytohormones and carbohydrate metabolism at different anther stages under DS and provide novel insight into molecular mechanisms of drought tolerance in tomato.